Affective Neuroscience

 Chapter 1

 Emotional Homology

At this point, it is important to focus a bit on the concepts of homology and analogy, especially as they apply to brain mechanisms. Homology is a term used in anatomy to indicate genetic relatedness of bodily structures. For instance, human arms and bat wings are homologous because they both arise from the genetic information that controls forelimb development. Although the functions have diverged markedly, one can still get a great deal of insight about the use of human forelimbs by analyzing the arm movements of any other mammalian species. On the other hand, the wings of birds and bees are analogous—serving a similar function—even though they do not share a common genetic inheritance. In a strict sense, these are morphological terms used to discuss body structures, and they should not be used to discuss such issues as brain functions. However, the neuroanatomical and neurochemical similarities in the underlying behavioral control processes are presently sufficient to lend great credence to the likelihood that pervasive homologies are present in these types of basic psychoneural functions in all mammals.

 Chapter 2

All mammals, indeed all organisms, come into the world with a variety of abilities that do not require previous learning, but which provide immediate opportunities for learning to occur. The influence of these systems varies as a function of the life span in each species (Figure 2.1). Analysis of the emotion systems that control behavior is complicated by the fact that the intrinsic arousability of underlying brain systems may change in many ways as organisms age. Still, the present premise will be that emotional abilities initially emerge from “instinctual” operating systems of the brain, which allow animals to begin gathering food, information, and other resources needed to sustain life. As such emotive systems mature and interact with higher brain areas, where they undergo both rerepresentation and refinement, organisms learn to make effective behavioral choices. Emotional tendencies such as those related to fear, anger, and separation distress emerge at early developmental stages, allowing young animals to cope with archetypal emergency situations that could compromise their survival. Gradually, through their effects on other parts of the brain, these systems allow animals to have more subtle social feelings and to anticipate important events and deal with them in increasingly complex ways. Others, such as sexual lust and maternal devotion, emerge later to promote reproductive success. Additional social processes, such as play and the seeking of dominance, start to control behavior with differential intensities during later phases of life and help promote the establishment of stable social structures and the propagation of the most fortunate and the most able.

In addition to responding to emergency situations, mild arousal of these brain systems presumably helps generate characteristic moods and coaxes animals to perform their everyday activities in characteristic ways. Even when there is no clear environmental reason for emotional arousal, these systems may continue to prompt organisms to undertake new activities (as in the case of exploration or play), all the while providing internal values (i.e., positive and negative feelings) for life choices.

The most primal affective-cognitive interaction in humans, and presumably other animals as well, is encapsulated in the phrases “I want” and “I don’t want.” These assertions are reflected in basic tendencies to approach and avoid various real-life phenomena. However, there are several distinct ways to like and dislike events, and a proper classification scheme will yield a more complex taxonomy of emotions than the simple behavioral dimension of approach and avoidance. For instance, it seems unlikely that the dislike of bitter foods and the dislike of physical pain emerge from one and the same avoidance system. It is equally unlikely that the desire for food and the urge to play emerge from the same brain systems.

Instrumental or operant conditioning occurs when animals begin to emit seemingly “intentional” or “voluntary” responses to obtain certain changes in the environment, such as the avoidance of negative events or the occurrence of positive ones. The trick to generating the fastest and most successful forms of operant conditioning is to rely on response systems that animals use spontaneously in their everyday interactions with the world. Animals are most likely to emit conditional instrumental responses by molding preexisting tendencies within their spontaneous behavioral repertoires. For instance, a rat’s FEAR system can produce unconditional freezing and flight, which are quite easy to obtain during simple contextual fear conditioning. Simply giving an animal a foot shock in a test box is sufficient to evoke freezing whenever the animal is returned to that environment. However, if the animal has an avenue of flight, it will rapidly learn to escape the situation. By comparison, it is difficult to train rats to press a lever to avoid foot shock. Such responses are quite unnatural for the animal.

 Flexible Intrinsic Behavior

The existence of intrinsic but behaviorally flexible brain systems has been repeatedly demonstrated by investigators of animal behavior, in simple and elegant experiments. For instance, most young birds do not learn to fly. They will fly at the appropriate age (i.e., maturational stage) even when deprived of the opportunity to exercise such skills prior to their first flight. But they still need to learn where to fly. A similar pattern is seen with rough-and-tumble play: Young rats do not need early experiences with play in order to exhibit outwardly normal ludic interactions as juveniles. But they still need to learn which moves are most effective.
Of course, the expressions of most intrinsic behavior control systems are intermediate: Intrinsic components are rapidly modified by procedural learning. For instance, whereas the courting songs of some avian species appear to be largely innate, other species acquire their characteristic song with the help of learning. They must be exposed to the song of their species when they are young so as to have an appropriate memory template later in life for generating their species-characteristic song. Indeed, the acquired template of some species is so flexible that members will try to imitate the songs of other species if these are all they have heard during critical periods of early development. As always, most behaviors are intermixtures of innate and learned tendencies.
Consider the reaction of cats to one of their natural prey objects, rodents. Their predatory system is based in part on innate tendencies, but these can easily be counteracted by early experiences. Most cats that have been reared only with other cats will hunt and kill mice and rats, but those that have been reared with rats from the time of birth show no such inclination. ...At some point in brain evolution, behavioral flexibility was achieved by the evolution of conscious dwelling on events and their meaning, as guided by internally experienced emotional feelings. I will argue that these emotional values are a fundamental property of emotional command systems, and that such values are instantiated by “raw feels”—the various forms of affective consciousness that all mammals can experience in the intrinsic neurodynamics of their brains/minds when specific neurochemical systems of the brain become active.

 Fundamental Life Tasks

Affective experiences are internally generated by neuronal mechanisms that arose to respond to categories of life-challenging events that bombarded our ancestors during the long course of brain evolution. For instance, hunger helps signal energy depletion, not necessarily because immediate energy reserves are dangerously low but because certain forms of energy depletion were encoded as affective anticipatory tendencies within the brain during untold aeons of evolutionary development. In other words, it is more adaptive to anticipate future energy needs than to respond simply to energy emergencies when they arise. ...Emotions, especially when they connect up with learning mechanisms, also appear to have this type of anticipatory character. ...It is safer and wiser to anticipate possibilities rather than to deal with them once they are squarely in your face.

...Descartes’s third rule for the scientific pursuit of knowledge: “To think in an orderly fashion when concerned with the search for truth, beginning with the things which were simplest and easiest to understand, and gradually and by degrees reaching toward more complex knowledge, even treating, as though ordered, materials which were not necessarily so.”

 Behavior Mixes Innate and Learned

All behavior in mammals, at least from the moment of birth, is a mixture of innate and learned components.

Although emotional traits can be selectively strengthened or weakened by breeding as well as by cross-rearing in animal experiments, comparatively little has been done with a direct neural end point... Other recent work has shown that neurochemical profiles of the brain can be inherited in both animals and humans.

 Chapter 4

 Subcortical Homologies

Fortunately, if one learns the subcortical neuroanatomy of one mammalian species, one has learned the ground plan for all other mammals. Indeed, by mastering the brain of one mammal, one immediately enjoys a good understanding of the subcortical neuroanatomy of most other vertebrate species. This is direct evidence for many structural homologies in the brain, which helps justify the belief that many brain functions are also homologous across species.

...the thalamic-neocortical axis of the somatic nervous system...harvests information from our external bodily senses and guides our skeletal motor systems through the cognitive influences of appraisals, plans, and other representations of the outside world.

 Open and Closed Neurological Systems

We should always keep in mind a key conceptual distinction when we consider brain operating systems, namely, how “open” or “closed” are these systems in relation to environmental influences (Figure 4.2)? For instance, very simple reflexive behaviors such as yawning and eye blinking are typically considered to be “closed”—they operate in much the same way every time, with a characteristic time course and intensity. In humans, even such reflexive events are not completely closed and can be substantially modulated by environmental events.

 Triune Brain

MacLean divided a vast architecture into three layers of evolutionary development: (1) the ancient reptilian brain, which elaborates the basic motor plans animals exhibit each day, as well as primitive emotions such as seeking, and some aspects of fear, aggression, and sexuality; (2) the more recent old-mammalian brain, or limbic system, which increases the sophistication of basic reptilian emotions such as fear and anger, and most especially elaborates the social emotions; and (3) the most recent addition, the neomammalian brain, consisting largely of the neocortex, which elaborates prepositional logic and our cognitive/rational appreciation of the outside world. ...Even though many specialists have criticized the overall accuracy of the image of a “triune brain,” the conceptualization provides a useful overview of mammalian brain organization above the lower brain stem.

 Relation of Neocortext to Midbrain Instincts

In other words, the mere removal of the neocortex does not lead to major deficits in instinctual behaviors, although such animals are certainly not very bright. ... The brain is a hierarchical system (see Figure 2.2). Higher functions can operate only on the basis of lower functions; but quite often lower functions can operate independently of higher ones. Since the lower functions are essential, it is understandable why brain stem damage is generally more debilitating than cortical damage. Higher functions are typically more open, while lower ones are more reflexive, stereotyped, and closed. ... Surgical removal of the cerebral hemispheres (i.e., decerebration) as well as certain cortical regions makes animals temperamental, with prominent bouts of rage in reaction to minor irritations.

There are operating systems for exploration, aggressive defense, fear, and various social initiatives, all of which can be demonstrated at the midbrain level.

 Cortical Control

Cortical control of primitive behaviors and basic emotions has been achieved in several ways. One way was for the cortex to extend emotions in time by allowing organisms to dwell on past and future events. Another pervasive solution was for the cortex to inhibit the actions of primitive instinctual systems situated in subcortical areas. For instance, all humans have circuits within their brains that can instigate intense rage, but it is rare for such impulses to control our outward behavior. However, if certain areas of the cortex are destroyed, these potentials are more likely to emerge as actions. The cortex not only helps keep simpleminded impulses under control but presumably permits selective and refined expression of primitive tendencies. This makes our brains resemble old museums that contain many of the archetypal markings of our evolutionary past, but we are able to keep much of that suppressed by our cortical lid. Our brains are full of ancestral memories and processes that guide our actions and dreams but rarely emerge unadulterated by corticocultural influences during our everyday activities.

 Decorticate Animals

Decorticate animals continue to exhibit their instinctive behavior patterns.

 Decerebrate Temperament

Surgical removal of the cerebral hemispheres (i.e., decerebration) as well as certain cortical regions makes animals temperamental, with prominent bouts of rage in reaction to minor irritations. Since such animals do not always direct their temperamental energies correctly (to appropriate targets), their emotional displays were often deemed to be “pseudoaffective.”

 Temporal Lobectomy

Temporal lobectomy made animals hypersexual, hyperoral, and less fearful—the so-called Klüver-Bucy syndrome, which is also evident in humans.

 Chapter 5

David Hubel and Torsten Wiesel were the first to demonstrate that neurons in the visual cortex are tuned to receive such specific types of information as the orientation of lines and edges and their movements in specific directions. These highly tuned sensitivities are thought to constitute the basic neuronal grammar of vision.

One remarkable finding of such research has been that the frontal cortex and basal ganglia elaborate motor plans, and that one specific area of the brain, the supplementary motor area (SMA), seems to always participate in the initiation of movement, and hence intentionality. Neuronal activity in the SMA predictably precedes voluntary motor actions.

While norepinephrine and serotonin cells “sleep” when we sleep, dopamine neurons remain prepared to fire at high rates during all of our various vigilance states, and all of the above neurochemical systems exhibit increased firing during emotionally aroused waking states.

 Brain Waves

At present, five general categories of brain waves are recognized in humans. The slowest rhythm is delta (0.5-3 Hz), which generally tends to reflect that the subject is sleepy (see Chapter 7). The next is theta (4-7 Hz), which has been related to meditative experiences, unconscious processing, and some negative emotional effects such as frustration. However, as mentioned, theta reflects active information processing in certain brain areas such as the hippocampus (HC). When this rhythm occurs in the HC, an organism is typically exploring and the HC is presumably elaborating thoughts and memories. This rhythm is also characteristic of the HC during rapid eye movement (REM) sleep (see Chapter 7). The brain’s relaxed, or “idling,” rhythm is alpha (8-12 Hz), which provides an excellent reference measure for detecting changes in brain arousal. In other words, the ongoing electrical energy in the alpha range can be used as a baseline for detecting how various brain areas become aroused during specific cognitive tasks and emotional situations. Beta rhythm (typically 13-30 Hz) is generally considered an excellent measure of cognitive and emotional activation. Finally, oscillations above beta are usually considered to be in the gamma range (i.e., more than 30 Hz); they are presently thought to reflect some of the highest functions of the human brain, such as perceptual and higher cognitive processes. With modern computational techniques, one can easily segregate the various frequency bands (through a mathematical procedure called Fourier analysis); one can estimate the power (or amplitude) within the component waves and highlight their coherence (i.e., synchronization) at different brain sites.
Individuals differ greatly in the characteristic types of brain wave parameters they exhibit. For instance some have a great deal of alpha and others comparatively little; others are rich in theta while most are not. The manner in which these fairly stable differences relate to personality has not been determined, but one possibility is that those with a great deal of alpha tend to be “laid-back,” concept-oriented people, while those with a predominance of beta are more “action-type,” detail-oriented people. Other personality relationships have been suggested, but more work must be done before such ideas can be accepted. EEG techniques have been most valuable in allowing neurologists to study various brain disorders, the most prominent being epilepsy, which can be monitored with scalp electrodes, since seizures are accompanied by rhythmic, high-amplitude delta waves that are never seen during normal states of consciousness.

Another important measure is that of coherence, or temporal correlation, between brain waves recorded from distant sites. If brain waves are moving together rather than independently, in the absence of an epileptic seizure, it is assumed that those areas are coordinating their activity.

Chaos theory has now been able to provide insights into the orderly patterns that operate in a variety of seemingly random processes. A main characteristic of such systems is that initial conditions are very important for the eventual patterns that emerge, while seemingly small influences can have far-reaching consequences. Following even mild perturbations, chaotic systems can fall into new, seemingly unpredictable, states of organization. However, it can be demonstrated that the seeming random patterns are in fact still governed by “attractors”—systemic properties that generate complex but repetitive patterns. Such approaches are having a growing impact on the analysis of complex physiological systems, including brain electrical activities.
...As a first approximation, it might be suggested that the various basic emotional circuits of the brain can serve as potential “attractors” for distinct types of neural activity in other parts of the brain. Thus, when an organism becomes emotionally aroused, neural ensembles throughout the brain may become captivated into certain repetitive firing patterns, thereby promoting the retrieval of a variety of stored memories and other brain processes relevant for each emotional state. ...Through the influence of emotional attractors, organisms may rapidly shift into any of a variety of waking states depending on rapidly changing environmental events.

It is known that individuals with temporal lobe epilepsy tend to develop characteristic personality disorders. For instance, one of the most famous historical cases is that of the great Russian novelist Fyodor Dostoyevsky (1821-1881), who developed a chronic seizure disorder following his arrest for participating in socialist intellectual activities in the middle of the 19th century. After being taken to the place of execution, presumably to be shot, he was given a reprieve at the last moment (a form of emotional terror the czar sometimes used to keep creative people in line). Unfortunately for Dostoyevsky, but fortunately for world literature, the ensuing post-traumatic stress disorder that developed during his exile in Siberia was manifested, for the rest of his life, by what we now recognize to be an acquired temporal lobe seizure disorder. The accompanying neuropsychological changes promoted powerful feelings of ecstatic delight and demonic despair that permeated much of Dostoyevsky’s anguished life and literary output.
It is noteworthy that similar experimentally induced epilepsies can also produce permanent personality changes in animals. In an experimental procedure known as kindling, animals are induced to exhibit epileptic states by the periodic application of localized electrical stimulation to specific areas of the brain. The term kindling comes from the gradual induction of this permanent brain sensitivity. The amygdala, an emotion-mediating brain area, is an ideal site for kindling studies, since seizure activity can be induced here most rapidly. The procedure consists simply of applying a burst of brain stimulation through indwelling electrodes for a period of one second, once a day, for a week or two. After the first brief ESB, nothing special happens... After a week or so, the brief stimulation produces a full-blown motor fit, unambiguous both behaviorally and in the poststimulation EEG. Thereafter, the animal will always have a seizure when it receives this burst of brain stimulation. Gradually even other stimuli become capable of triggering seizures, especially loud sounds and flashing lights.

It is clear that people often have distinct types of EEG patterns, but definitive conclusions are difficult to derive from the empirical literature. However, one consistent theme with regard to emotionality and EEG changes has recently been emerging. Several laboratories have now demonstrated that happy feelings, even sustaining a voluntary but sincere smile, will induce arousal (alpha blocking) in left frontal areas of the brain,71 while unhappy feelings, including disgust, will evoke larger arousal in right frontal areas.72 Indeed, individuals who are prone to depression tend to exhibit more right frontal arousal than those who are not.73 These patterns can be observed even in babies. Indeed, infants who exhibit the highest arousal in right frontal areas tend to be the ones who are most likely to cry in response to brief periods of maternal separation.
These brain changes are consistent with the emotional changes that have commonly been observed in humans following right and left hemisphere strokes (also see Chapter 16). The right hemisphere becomes aroused in response to negative emotions, and damage here typically has few negative emotional consequences; often, patients remain cheerful despite the severity of their problems. On the contrary, comparable damage to the left frontal areas, which become aroused in response to positive emotions, can cause catastrophic emotional distress, and such patients are more prone to become despondent and depressed.

 Chapter 6

A remarkable number of receptors have similar transmembrane domains, which reflects the fact that they have shared a long evolutionary history. Since invertebrates typically also have homologous receptors, they must have first emerged in brain evolution a very long time ago. Indeed, we can estimate divergence times of species by counting up the number of amino acid changes that are contained in receptors, as well as all of the other long proteins of the body...

It is noteworthy that no neurotransmitter or neuromodulator has been discovered in humans that is qualitatively different from those found in other mammals. In fact, all mammals share remarkably similar anatomical distributions of most neurochemical systems within their brains.

 Exaptation

When evolution uses existing functions for new purposes, the end result is typically called an exaptation. For instance, the use of gill arches to construct jawbones was such a transition. The use of some of those bones to construct the inner ear is another classic example. ...we should always remain alert to the possibility that what we might be tempted to interpret as a functional homology might actually be an exaptation that is far removed from the ancestral function. If that is the case, no special cross-species functional generalization can be derived. Thus, arguments by homology must always be evaluated empirically.

 Lack of Parsimony In Neurology

It is not uncommon for a single neurochemical system, or a single psychoactive drug, to have effects on nearly every behavior that is measured. For instance, the list of behavioral functions that brain serotonin does not modify is very short, containing no items, whereas the list of functions serotonin does affect includes everything the animal does.12 Essentially the same conclusion holds for ACh, dopamine (DA), norepinephrine (NE), glutamate, and GABA. This indicates that many transmitters can exert global effects on brain and psychological functions, but there are some consistent patterns with regard to the direction of change. For instance, facilitation of serotonin typically suppresses behavior, while drugs that promote DA, NE, and ACh activity typically facilitate behaviors. As would be expected of molecules that modify moods and emotions, such changes modify everything an animal does. By comparison, steroid and peptide neuromodulators often have more precise behavioral and emotional effects...

In this role, catecholamines probably influence performance in a classic inverted U-shaped fashion: Behavior increases from the initial point of arousal up to a certain level and then diminishes as excessive arousal begins to preclude behavioral flexibility. This relationship is commonly called the Yerkes-Dodson law._43 Thus, with excessive DA activity, animals begin to exhibit repetitive behavior patterns known as _stereotypies; with low NE activity, they tend to perseverate on a task despite changes in stimulus contingencies (presumably because of attentional deficits). Without adequate cortical NE, organisms are also prone to act impulsively rather than deliberately.

All motivated and active emotional behaviors, including feeding, drinking, sex, aggression, play, and practically every other activity (except sleep), appear to be reduced as serotonergic activity increases.

As recent work has clearly indicated, many children with autism have a brain disconnection syndrome, especially between cerebellar and limbic zones with other higher brain areas. In other words, neural systems that should be working in close unison appear not to have developed normal synaptic interchange in various brain areas that control socialization, communication, and imagination.

It is likely that certain addictive behaviors in humans, such as compulsive gambling, are strongly controlled by internal urges that are generated by dopamine chemistries.

Psychologists have traditionally had a difficult time generating a satisfactory definition of “stress.” In psychobiology, it is much easier: Stress is anything that activates the pituitary-adrenal system (the ACTH-cortisol axis). Everything that is typically considered to be a stressor in humans generates this brain response.

If cortisol secretion is sustained at excessive levels, the metabolic resources of hippocampal neurons become depleted and die prematurely. In short, a sustained stress response can kill certain brain cells! ...Since brain cells are not replaced, this can pose a serious problem for subsequent cognitive abilities.

...the peripheral autonomic nervous system has long been recognized as the output system for emotions.

 ADD Kids and Decorticate Animals

[ADD] children have too little cortical arousal, which permits their subcortical emotional systems to govern behavior impulsively. When cortical arousal is facilitated with psychostimulants, ADD children are able to better utilize their attentional abilities to stay on task. In other words, ADD kids resemble decorticate animals, which are also hyperactive and jump rapidly from one activity to another.

 Part II Intro

It is becoming increasingly clear that humans have as many instinctual operating systems in their brains as other mammals. However, in mature humans such instinctual processes may be difficult to observe because they are no longer expressed directly in adult behavior but instead are filtered and modified by higher cognitive activity. Thus, in adult humans, many instincts manifest themselves only as subtle psychological tendencies, such as subjective feeling states, which provide internal guidance to behavior.

The basic emotions appear to arise from executive circuits of the brain that simultaneously synchronize a large number of mental and bodily functions in response to major life-challenging situations. Although many emotional nuances can be “socially constructed” by the human mind, usually designed by the textures of specific human cultures, the affective strength of the basic emotions arises from intrinsically “motivating” neurophysiological properties of genetically ordained subcortical emotive systems.
Since brain emotive systems were designed through evolutionary selection to respond in prepared ways to certain environmental events, it often seems from our “mind’s-eye” perspective that world events are creating emotions as opposed to just triggering evolutionarily prepared and epigenetically refined states of the brain. In fact, many of the feelings and behavioral tendencies that characterize the basic emotions reflect, more than anything else, the intrinsic, genetically prepared properties of brain organization.

 Chapter 7

Indeed, many emotion-mediating areas of the brain “light up” during REM, but one surprise has been that the prefrontal areas, which generate active plans, remain quiescent, as they do during SWS.

Although we do not presently know exactly how memories are consolidated during REM, we can anticipate that the hippocampus will be in the middle of the neuronal action. After all, the hippocampus is the brain area that is well established to be a mediator between short- and long-term memories, and it goes into a characteristic theta state during REM

The massive PGO neuronal discharges are accompanied by REMs, bodily jerks, and muscular tremors that break through the motor inhibition and often resemble fragments of motivated/emotional behaviors (e.g., weak barks and snarls in dogs, with slight running movements of the paws, which presumably reflect their dream content).

Brain mechanisms that evolved earlier are typically lower within the neuroaxis and in more medial positions than more recent additions.

In other words, animals appear to be evolutionarily prepared to learn such simple emotional tasks.

Probably the most striking and highly replicable neurochemical finding in the whole psychiatric literature is that individuals who have killed themselves typically have abnormally low brain serotonin activity.

 Chapter 8

Now we know that ascending DA tracts lie at the heart of powerful, affectively valenced neural systems that allow people and animals to operate smoothly and efficiently in all of their day-to-day pursuits. These circuits appear to be major contributors to our feelings of engagement and excitement as we seek the material resources needed for bodily survival, and also when we pursue the cognitive interests that bring positive existential meanings into our lives. Higher areas of the motor cortex are also energized into action by the presence of DA. Without the synaptic “energy” of DA, these potentials remain dormant and still. Without DA, human aspirations remain frozen, as it were, in an endless winter of discontent. DA synapses resemble gatekeepers rather than couriers that convey detailed messages. When they are not active at their posts, many potentials of the brain cannot readily be manifested in thought or action. Without DA, only the strongest emotional messages instigate behavior. When DA synapses are active in abundance, a person feels as if he or she can do anything. Is it any wonder that humans and animals eagerly work to artificially activate this system whether via electrical or chemical means?

...in this chapter I will pursue the idea that the mammalian brain contains a “foraging/exploration/investigation/curiosity/interest/expectancy/SEEKING” system that leads organisms to eagerly pursue the fruits of their environment—from nuts to knowledge, so to speak. Like other emotional systems, arousal of the SEEKING system has a characteristic feeling tone—a psychic energization that is difficult to describe but is akin to that invigorated feeling of anticipation we experience when we actively seek thrills and other rewards.

This system responds unconditionally to homeostatic imbalances (i.e., bodily need states) and environmental incentives. It spontaneously learns about environmental events that predict resources via poorly understood reinforcement processes (Figure 8.1).

 Locating Seeking in the Brain

I believe that these transhypothalamic circuits lie at the very heart of the SEEKING system. The LH continuum, running from the ventral tegmental area (VTA) to the nucleus accumbens, is the area of the brain where local application of electrical stimulation will promptly evoke the most energized exploratory and search behaviors an animal is capable of exhibiting.

 Naming Seeking

Originally I called it the foraging/expectancy system, while Jeffrey Gray called it the behavioral activation system;_3 more recently, Richard Depue chose to call it the _behavioral facilitation system, and most investigators now working in the field are beginning to agree that it is a general “incentive or appetitive motivational system” that mediates “wanting” as opposed to “liking.”
...SEEKING seems to be a more suitable term for psychology because it implies a distinct psychological dimension as opposed to a mere behavioral process. This harmoniously operating neuroemotional system drives and energizes many mental complexities that humans experience as persistent feelings of interest, curiosity, sensation seeking, and, in the presence of a sufficiently complex cortex, the search for higher meaning.

 Seeking and Causation

Although this brain state, like all other basic emotional states, is initially without intrinsic cognitive content, it gradually helps cement the perception of causal connections in the world and thereby creates ideas. As we will see, it appears to translate correlations in environmental events into perceptions of causality, and it may be a major source of “confirmation bias,” the tendency to selectively seek evidence for our hypotheses.

The affective state does not resemble the pleasurable feelings we normally experience when we indulge in various consummatory behaviors. Instead, it resembles the energization organisms apparently feel when they are anticipating rewards.

Traditionally, all motivated behaviors have been divided into appetitive and consummatory components. This distinction is premised on the recognition that one must not only seek out and approach the material resources needed for survival (except for oxygen, of course) but also interact with them in specific ways once they have been found: One must eat, drink, copulate, or carry the desired items home. The SEEKING system appears to control appetitive activation—the search, foraging, and investigatory activities—that all animals must exhibit before they are in a position to emit consummatory behaviors.

In other words, the SEEKING system is initially activated by the unconditional distal incentive cues of rewards, such as smells and sights; eventually, through learning, neutral cues can come to arouse and channel activity in this system through a reinforcement process that is linked to the inhibition of approach in some presently unknown manner (as schematized in Figure 8.1). In other words, the search system automatically evaluates the importance of environmental events and stores that knowledge for future use, perhaps through some type of “reinforced” memory process.

In one of the first studies to measure neuronal action potentials within the trajectory of the SEEKING system, it was found that neurons were typically aroused in the LH when animals were searching for food and shut down promptly when the food was found and feeding began. In other words, the appetitive phase of behavior corresponds to high arousal of the LH system, while consummatory pleasures are more closely related to offset of neuronal activity in this system. This type of finding has been affirmed by a great deal of subsequent research.

...it is now evident that the LH behavioral arousal SEEKING system is much more devoted to anticipatory-appetitive arousal rather than simply to consummatory reward processes, which are even more ancient functions of the brain.

When tested in such an arena without any brain stimulation, cats spent significantly more time investigating the area where the [LH] stimulation had gone off rather than the area where it had come on! These results suggest that the offset signaled psychological relevance or positive reward value more than the onset. At the very least, the “off location” ranked higher in the animal’s internal interest hierarchy than the “on location.”

Behavior induced by LH stimulation most clearly resembles the type of arousal that animals exhibit in the presence of cues predicting the availability of appropriate rewards, such as a dog expressing eagerness at the sight of the leash that signals a walk or the sound of a can opener that signals forthcoming food.

In fact, when animals eat, drink, or have sex there appears to be a chaotic, dancelike tension between the consummatory and appetitive phases of behavior. As the animal momentarily settles down to eat, each swallow is followed by the urge to reach out for more.

This is especially important since many investigators who discuss human emotions have had difficulty agreeing what emotional state this system is supposed to mediate. I would suggest that “intense interest,” “engaged curiosity,” and “eager anticipation” are the types of feelings that reflect arousal of this system in humans.

That [the Seeking] system is innate is indicated by the ability to obtain SS in neonatal rats. The system is not dependent on higher brain functions, for it continues to operate effectively in adult animals even though most of their higher cognitive mechanisms have been surgically removed.

If the [Seeking] system is damaged, a generalized behavioral inertia results; if the system is stimulated, either pharmacologically or electrically, a large number of motivated behaviors and a variety of physiological changes are invigorated.

Subsequent investigators demonstrated that these unusual behaviors could be more simply explained by a single factor—-an “incentive” process independent of normal homeostatic imbalances (i.e., the drive state) that normally tend to sensitize responsivity to potential sources of external rewards.

At present, it is essential to conceptualize an incentive process—a fundamental appetitive motivation process—as an intrinsic brain function.

Then Elliot Valenstein and his colleagues did a series of experiments with “stimulus-bound” feeding, drinking, and gnawing that startled the behavioral neuroscience community. These results laid to rest the simpleminded mechanistic hope that distinct circuits would be found in the LH for all the observed consummatory behaviors. The experiments indicated that the hypothalamic motivational system that was activated when animals exhibited distinct behaviors was nonspecific. The LH apparently mediated some process other than the specific behaviors that were being observed!

Furthermore, it was demonstrated that the animal’s emotional temperament could predict what type of stimulus-bound behavior it would exhibit. Rats would exhibit “stimulus-bound” predatory behavior, such as attacking mice, only if they already had a natural tendency to indulge in it. Animals that appeared especially likely to exhibit what ethologists call “displacement activities” (motivational spillover between emotive systems) were most likely to exhibit strong appetitive behaviors.

Even though animals are prone to exhibit many distinct consummatory behaviors when this system is activated, depending on their “personality” tendencies and bodily needs, there is one behavior that is exhibited by all. All animals move forward in an energetic search pattern, sniffing vigorously and investigating, mouthing, and manipulating prominent objects in the environment.

Several investigators configured experimental situations in such a way that ESB was applied only when the animal was on one side of a test chamber, the side that had been provisioned with a variety of “junk” objects, while the other side, where stimulation went off, was empty. After some experience with this situation, most animals begin to systematically carry the objects from the stimulation side to the no-stimulation side. The end result was that the pile of junk was transferred from one side of the chamber to the other. One way to understand this is to surmise that LH stimulation arouses a brain state that normally occurs when animals forage for worldly goods outside of their home burrow, and that animals tend to drop objects when this type of neural activity ceases:

In sum, data from in vivo neurochemical analyses have confirmed that the activation of DA systems is related more closely to the appetitive than to the consummatory phase of motivated behavior. However, the possibility that this system also responds to stressors and the anticipation of aversive events has received provisional support, suggesting that it responds not simply to positive incentives but also to many other emotional challenges where animals must seek solutions.

Behavioral variety is further promoted by the motivationally generalized SEEKING system because it can be modulated by a variety of specific homeostatic detectors within medial strata of the hypothalamus. As will be summarized in the next chapter, many need-specific regulatory systems in the hypothalamus can modulate the arousability of the SEEKING system. Interoreceptive neurons, which detect water, energy, thermal, and other imbalances, energize the search for vital resources in part by promoting the arousability of the SEEKING system.

This pattern of results suggests that the LH-SS or SEEKING system is one of the first brain areas to learn an appetitive task, and in well-trained animals it is among the first to express its learning. These results suggest that a fundamental appetitive learning mechanism, which generates positive expectancies, resides within the lateral hypothalamic tissue.

Specifically, on a FI schedule, where the possibility of obtaining reinforcement occurs only at set times, animals tend to withhold their responses during the first half of each postreward interval, and operant behavior increases gradually during the second half of the interval, before there is any realistic opportunity to obtain rewards. Thus, animals appear to be natural “optimists,” invariably underestimating the amount of time they need to wait. ...Although behaviorists are loath to use terminologies such as expectancies,78 it seems as if animals working on FI schedules exhibit a gradual intensification of behavioral excitement, or anticipation, as each interval draws to a close.

Thus, the brain system that generates sniffing became engaged a moment before the animal emitted its first operant responses. This suggests that the spontaneous arousal of the SEEKING system helped arouse the instrumental behavior.

Presumably, these same systems allow us to develop a sense of causality from the perception of correlated environmental events. This type of spontaneous associative ability characterizes normal human thinking, as well as the delusional excesses of schizophrenic thinking.

Arousal of the SEEKING system spontaneously constructs causal “insights” from the perception of correlated events. Some of the relationships may be true, but others are delusional. Indeed, all forms of inductive thought, including that which energizes scientific pursuits, proceed by this type of logically flawed thinking (see Figure 2.3). An intrinsic tendency for “confirmation bias” appears to be a natural function of both human and rat minds.

In the classic demonstration of this phenomenon, pigeons were exposed to an illuminated key just prior to the delivery of food. With repeated exposure to this contingency, pigeons exhibited anticipatory pecking at the illuminated key, even though there was no formal connection between anything the animal did and the appearance of food. It was as if the animal believed its behavior was instrumental in procuring the food, although, in fact, it was not. Of course, this is a very effective way to train animals to do various things, even though at a formal level such behaviors reflect delusional thinking. Comparable phenomena have now been observed in all mammalian species that have been studied. The “rain dances” of Indian shamans and the prayers of the devout may reflect such processes in humans. If performed long enough, such rituals are bound to “work,” even though there may be no causal relationships between the dances or prayers and events in the world.

Another bizarre behavior generated by the SEEKING system is schedule-induced polydipsia (SIP). This is the excessive drinking that can be produced in hungry rats by giving them small portions of food on an FI schedule; using about two-minute intervals between food delivery produces the maximal response. If water is not available, the animal will exhibit other behaviors such as compulsive shredding of available objects or schedule-induced wheel running. One can even obtain aggression if another animal is nearby. Animals appear to vent the frustration of neuroemotional energy emerging from unfulfilled expectations on any available target.

Thus, the SEEKING system can promote many distinct motivated behaviors, and the underlying neural system is prepared to jump to the conclusion that correlated environmental events reflect causal relationships. It is easy to appreciate how this may yield a consensual understanding of the world when the underlying memory reinforcement processes are operating normally (i.e., yielding a “reality” that most of the social group accepts). It is also easy to understand how it might yield delusional conclusions about the world. If the system is chronically overactive, it may be less constrained by rational modes of reality testing.

 Chapter 9

Mammals can survive only if they maintain relative constancy of various bodily processes, including oxygen and carbon dioxide content in blood, body water levels, salt and energy balance, and body temperature. Complex brain and body systems sustain these constancies, and the overall concept used to describe this ability is homeostasis.

Bodily needs instigate distinct forms of bodily arousal and psychological feelings of distress such as hunger, thirst, and coldness. Animals have exquisite sensory systems to identify the most important items they need—for example, the ability to taste sweetness identifies foods laden with sugar, and saltiness identifies sources of sodium. It is commonly believed that color vision evolved, in part, to help primates identify the ripest fruit.

Sensations generate pleasure or displeasure in direct relation to their influence on the homeostatic equilibrium of the body. For instance, if one is depleted of energy resources, foods taste better than when the body is already replete with energy.

Conversely, it should be noted that virtually all emotional states affect the intensity of our motivations. Most animals, even humans, are unlikely to eat much or exhibit any inclination for play or sex when they are very scared or angry. One long-term emotion that is especially incompatible with normal appetite is separation distress. When young animals are socially isolated, they typically lose weight even if they have free access to lots of food. When the young are reunited with their kin, and a mood of apparent contentment is reestablished, appetite returns.

Many bodily needs access the SEEKING system and thereby arouse appetitive search tendencies that motivate animals to approach and learn about available resources. It would have been wasteful for evolution to have constructed separate search and approach systems for each bodily need. The most efficient course was for each need-detection system to control two distinct functions: a generalized, nonspecific form of appetitive arousal and various need-specific resource-detection systems.

Thus, resource depletions within the body can lead to a generalized arousal of seeking behaviors regardless of the specific regulatory imbalances that exist, and specific need states that sensitize distinct consummatory reflex tendencies (e.g., licking, biting, chewing, and swallowing) and key support mechanisms, such as sensory, perceptual, and memory fields relevant for the specific needs. By the interplay of these processes, a generalized search system can efficiently guide animals to relevant environmental goal objects.

Existing evidence suggests that the SEEKING system is under the control of internal homeostatic receptor systems that detect various bodily imbalances. This is suggested by the fact that many imbalances can modify the rate at which animals self-stimulate lateral hypothalamic (LH) electrode sites. For instance, hunger reduces the current threshold needed to sustain LH self-stimulation while also increasing the rate at which animals behave. Similar effects can be evoked by thirst, cold, and various sex hormones, even though these have not been studied as thoroughly as the effects of food deprivation. ....Many of these [regulatory] neurons are sensitive to circulating nutrients such as amino acids, fatty acids, and blood sugar, or glucose.

 Differential Emotional Expression Across Species

It is important to note that electrode locations that readily yield self-stimulation in rats typically yield predatory aggression in cats. Obviously, this is a reasonable species-typical SEEKING behavior for a carnivorous animal that subsists at the top of the food chain. Outward behavior can sometimes mislead us about the functions of an underlying brain system. The failure to recognize this appears to have been another instance in which the variety of behaviors evoked by LH stimulation has deceived investigators about the generalized emotive functions of a brain circuit.

Incentive concepts may suffice, especially since specific deprivation states primarily facilitate an animal’s response to specific external incentive stimuli. Here, we will use the concept of a bodily need state as opposed to drive to indicate the presence of regulatory imbalances. For instance, need states such as energy depletion lead to dramatic increases in motor arousal only when animals are in the presence of incentive stimuli—namely, those stimuli that predict the availability and characteristics of relevant primary rewards such as food. At a physiological level, increased arousal can be measured by the intensification of reflexes as well as neural changes.
It should also be noted that there are problems with the traditional concept of incentive, as defined by the attributes of quantity, quality, and delay of reward. If the incentive process is defined only with respect to the external qualities of rewards, we may tend to overlook important properties of brain systems that evolved to respond to these attributes. In other words, the incentive process, as instantiated by specific properties of neural circuits, may respond to certain properties of external rewards so as to integrate an affective/motivational state within the brain. Once the incentive stimuli have interacted with such circuits, the aroused psychological response is only indirectly related to the outward properties of rewards.

In other words, the brain’s intrinsic, evolutionarily derived mechanisms add a new dimension to those inputs—namely, the incentive-directed psychobehavioral “energy” of the animal. The system sensitizes animals to respond vigorously when there are predictable rewards.

In addition, many other psychological processes, from fear to pleasure mechanisms, can easily subvert the brain’s regulatory actions for extended periods. For instance, fearful animals eat little. On the other hand, animals take large meals if their food is especially tasty but become finicky nibblers if it is not. They also take large meals if food is hard to find but tend to make many small meals if food is abundant.

Hunger produces a dramatic reduction in their play behaviors, as do other aversive states (see Figure 1.1), but a single meal brings play right back to normal.

The body’s daily energy cycle is largely regulated by the pancreatic secretion of insulin, the primary energy storage (anabolic) hormone.

Adult rats exhibit a remarkable ability to balance their body energy equation (Figure 9.4), and this is accomplished partly by metabolic changes on the output side of this equation. For instance, the regulation of energy output can be achieved by changes in muscular activity in addition to spontaneous changes in metabolism. However, a great deal is also accomplished on the input side, through changes in feeding behavior. ....The fact that energy balance is typically sustained over time suggests that the brain is sensitive to the overall flow of energy, and modifying factors on one side of the equation are balanced by compensatory changes on the other side.

We will find that this same area of the brain also controls female sexual receptivity (see Chapter 12), and it is important to note that reproduction is generally reduced by starvation conditions (it is not wise to have children when food is scarce!). The onset of female puberty is also triggered to some extent by weight (if one has abundant food, one should begin to reproduce earlier), which indicates how closely energy detectors and female sexual receptivity systems are coupled in the brain.

Rather, when animals are missing certain micronutrients, they feel unwell; when they encounter foods that restore those needed items, they feel healthier. Apparently animals are able to utilize restoration of health as a signal for the types of dietary choices they should make.

 Indirect Measurement of Emotions

Like the smile of the Cheshire cat, we can only glimpse feelings indirectly, for they are not tangible entities, and neuroscientists are prone to ignore neurodynamic processes that must be inferred. Of course, physics would be in a sorry state if physicists had ignored the internal dynamics of atoms.

The brain’s ability to generate a variety of subjective feelings during homeostatic imbalances may be nature’s way of providing a simple general-purpose coding device for discriminating the relevance of both external objects and internal states, thereby providing a powerful intrinsic motivational mechanism for guiding behavioral choices.

It has been experimentally affirmed that pleasant and unpleasant feelings provoked by external stimuli arise from their ability to predict the alleviation of bodily imbalances. Stimuli that promote a return to homeostasis are routinely experienced as pleasurable, while those that would impair homeostasis are unpleasant or even distressing.

In sum, pleasure is not simply a response to a specific environmental event but one that is guided by the internal status of relevant physiological systems. We are finally beginning to understand the nature of these homeostatic systems and the pleasure responses they evoke within the brain. A sweet taste that is deemed to be pleasant when one is hungry is not as pleasant if one has already eaten more than one’s fill. The same goes for sex and other forms of bodily touch (see Chapters 12 and 13). All these experiments point to one overwhelming conclusion: Pleasure is nature’s way of telling the brain that it is experiencing stimuli that are useful—events that support the organism’s survival by helping to rectify biological imbalances.

Animals that are given nonnutritive sweet solutions such as saccharin initially consume a great amount but gradually diminish their intake if they also do not have access to nutritive food. This suggests that the pleasure of taste is not sufficient to sustain consumption if it is not followed by beneficial metabolic consequences.

It also seems likely that opioid-mediated pleasure is a key ingredient in many other rewards. For instance, sexual reward has a strong opioid component. Male rats exhibit a place preference for locations in which they have copulated, but opiate receptor blocking agents decrease this preference, without reducing copulatory acts (see Chapter 12). There is evidence that opioids participate in the good feelings generated by maternal behavior and other social interactions involving touch (see Chapters 13 and 14). Indeed, brain opioids may participate in every pleasure, serving as a general neurochemical signal that the body is returning to homeostasis.

 Chapter 10

 Anger Triggers

Many stimuli can provoke anger, but the most common are the irritations and frustrations that arise from events that restrict freedom of action or access to resources.

 Anger and Aggression

In sum, aggression is a broader phenomenon than anger itself. Aggression is not always accompanied by anger, and anger does not necessarily lead to aggression, especially in mature humans who can control such base impulses.

 Kinds of Aggression

However, nearly all vertebrates exhibit aggression from time to time, and such behavior can have several distinct environmental and brain causes.
Three distinct aggressive circuits have been provisionally identified in the mammalian brain: predatory, intermale, and affective attack or RAGE circuits. Only the last one provokes enraged behaviors, and presumably the experience of anger. For instance, males that fight each other for access to sexual resources do not appear to be enraged but instead present themselves as potential champions on the field of competition. Of course, they may eventually become angry at each other as they lock horns. Likewise, predators kill other animals not out of anger but because they need food to live. We must assume that the hunt and the kill is as positive a psychological experience for the predator as it is a fearful one for the prey. Predatory attack is a distinct type of aggression that arises from different circuits than anger or the seasonal competition for dominance among males of “tournament species.” However, as we will see, it is not fully distinct from the SEEKING circuits discussed in Chapter 8.
... In addition to distinctions we can make among different forms of aggression, all forms share certain features, such as the potential for bodily injury and individual concerns about the distribution of resources. In humans, such resources may even be psychological ones. Because aggression entails many destructive potentials, intrinsic biological restrictions are placed upon it within all species (i.e., few animals, besides humans, kill other adult members of their own kind), and there are numerous societal sanctions against it in most human cultures. In general, there is much less aggression when animals have known each other for a long time than when they are strangers.
Animals in stable societies usually develop an acceptance of their social status, and hence their “rightful” priority in the line for resources, yielding dominance hierarchies. Among those that know each other, competition is often resolved by glances and gestures rather than blows. However, when organisms do not know each other, they are more likely to take the path toward physical confrontation and, if neither side backs down, bloodshed. At the cultural level, our laws attempt to ensure that humans do not impose their will on others; those who fail to comply with societal expectations are commonly recipients of various forms of societal retribution, which, with a modest stretch of the imagination, may also be defined as aggression.
At the outset, I wish to make one disclaimer: The most broadly destructive kinds of human aggression—wars between nations and competing cultural groups, as well as many violent crimes—do not arise directly from brain circuits of the type discussed here. These are instrumental acts that arise as willful activities of humans. Only weak precedents have been described in our kindred species, the chimpanzees, who occasionally exhibit group aggressive activities that resemble human tribal skirmishes, or miniwars, against others of their kind.3 Very little of what we have to say here can highlight the causes of similar instrumental political phenomena in human societies, except that aggression may seem like a reasonable strategy among those who have little to lose or much to gain.

 Anger Breeding

In any event, genetic selection experiments in both male and female rodents indicate that one can markedly potentiate aggressiveness through selective breeding within a half dozen generations, and that breeding for aggression is as effective in females as in males.

 Serotonin and Impulsivity

Likewise, animals and humans that have constitutionally low brain serotonin activity are more prone to aggression and the impulsive acting out of other emotions than those with higher levels. In addition, males are generally more aggressive than females partly because of fetal organizational and adolescent activational effects of testosterone on their brains (see Chapter 12).9 However, when it comes to defending their young, females of most species develop a propensity to become more defensive and assertive soon after giving birth. This may be partly due to a shift in brain chemistries within certain aggression circuits toward patterns that are more typical of males (see Chapter 13 for more on this topic).

 Male-typical Aggression

In many species, males are disproportionately larger than females (e.g., “tournament species,” such as elk and walruses, which seek to captivate many females in “harems”); especially high levels of intermale aggression are evident among such creatures. However, the fighting is typically restricted to the breeding season, when testosterone levels are particularly high.

 Baby Anger

For instance, a human baby typically becomes enraged if its freedom of action is restricted simply by holding its arms to its sides.

 Anger and Freedom Restriction

Anything that restricts our freedom will be viewed as an irritant deserving our anger, contempt, and revolutionary intent. Of course, restriction of freedom is not the only precipitant of our anger and scorn. The same response emerges when one’s body surface is repeatedly irritated or when one does not receive expected rewards, namely, when one is frustrated. ...
Perhaps one of the earliest evolutionary vectors was the adaptive advantage of having invigorated psychobehavioral responses to physical constraint, as commonly occurs in predator-prey encounters. Once a predator has captured its prey...[one] strategy is for the animal’s behavior to become vigorous very rapidly, which might startle or otherwise dissuade the predator from pursuing its course of action, thereby giving the prey a chance to flee and escape.

 Anger and Frustration

This simple observation suggests that unfulfilled expectancies within the SEEKING system activate the neural patterns of frustration, probably in frontal cortical areas, which compute reward contingencies. As will be explained in detail later, reward and expectation mismatches may promote anger by downward neural influences that arouse RAGE circuits.
Such cognitive precipitants of anger would, of course, require prior learning. By contrast, a young baby who becomes enraged because it is prevented from moving may not initially conceptualize the external source of its anger, but with social development and insights into the nature of social dynamics, it rapidly learns to appraise the sources of the irritations and frustrations in its world. And then the neural paths have been prepared for retributions.

 Anger Externalization

Indeed, human brains are evolutionarily “prepared” to externalize the causes of anger and to “blame” others for the evoked feelings rather than the evolutionary heritage that created the potential for anger in the first place.

 Submission Reduces Anger

Both psychologically and behaviorally, certain attitudes and gestures are especially efficacious in reducing anger. Among many types of animals, appeasement signals—for instance, lying on one’s back, exposing vulnerable parts like the belly and neck—commonly reduce aggression by others of the same species.

 Defensive Aggression

[Accompanying anger,] In the brain, there emerges an intense and well-focused tendency to strike out at the offending agent. The emotional state aroused in the brain is a fiery mental storm, capable of being defined in neurophysiological and neurochemical terms, that rapidly persuades us that the offending agent is below contempt and deserves harm. Previous memories related to the anger episode are easily remembered and potential plans for vengeance are automatically promoted.

 Frustration-Centric Anger

Since anger is most easily aroused when the availability of desired resources diminishes, it should have close anatomical and neurophysiological linkages to the SEEKING system. Indeed, arousal of the self-stimulation system entails an increased possibility of frustration, since this system establishes neural conditions for an affective state of high expectations and hence their failure to be met (Figure 10.1).
To the best of our knowledge, positive expectations, and the possibility of frustration, arise from neuro-dynamic activities of higher brain areas that compute reward contingencies—psychological processes that are linked intimately to the cognitive functions of the frontal cortex. A rapid suppression of activity within the SEEKING system, in the absence of homeostatic pleasures, which would normally index that a reward has been obtained, should unconditionally promote the arousal of anger circuitry. Indeed, such effects have been observed in animals’ elevated tendency to bite when rewarding brain stimulation is terminated.21 In comparable circumstances, humans tend to to clench their jaws and swear epithets. In other words, the RAGE and SEEKING circuits may normally have mutually inhibitory interactions (see Figure 3.5), even though both may be comparably sensitized by other processes such as the feelings of hunger aroused by the body’s energy needs. This makes psychological sense, since such need states would heighten the value of positive expectations, and hence the feelings associated with those expectations not being met.

Thus, the emotional feeling of frustration may largely reflect the mild arousal of RAGE circuitry, in the same way that anxiety may reflect weak arousal of the FEAR circuitry (see Chapter 11).

Certainly, the fact that patients with frontal cortical damage can become angry rapidly, but can also lose their anger rapidly, suggests that frontal cortical influences are important in sustaining instinctual anger responses that are elaborated by lower regions of the brain.

 Anger Facilitation

However, in this context it is important to remember that there are many other facilitators of aggression beside frustration—including hunger, pain, and perhaps some of the neural effects of testosterone.

For instance, the aggression that a mother exhibits to defend her offspring may not be fundamentally different from the aggression a male exhibits when an intruder infringes on his territorial “rights.” In both situations, aggression may be evoked by essentially one and the same brain circuit, even though the two can be distinguished taxonomically by the different psychosocial/cognitive precipitating conditions.

 Moyer Anger Taxonomy

The most widely cited behavioral taxonomy based on the eliciting conditions for aggression was developed by Kenneth Moyer. His list includes seven distinct forms of aggression: (1) Fear-induced aggression occurs when an animal cannot escape from an aversive situation; (2) a female often displays maternal aggression when an intruder is perceived to threaten the safety of her offspring; (3) irritable aggression results from annoying occurrences in the environment that are not strong enough to provoke flight; (4) sex-related aggression occurs in the presence of sexual stimuli; (5) territorial aggression occurs when a strange animal enters the living space claimed by a resident animal; (6) intermale aggression reflects the fact that two males placed together are much more likely to begin fighting than two females placed together; and (7) predatory aggression is a food-seeking mechanism in certain omnivorous and carnivorous species. One could even suggest others, such as play’-fighting, defensive aggression, and perhaps even lovers’ spats, but these types of distinctions are presently not very useful at the neuroscience level of analysis. (Moyer K.E. 1976 The psychobiology of aggression)

 Anger Distinction from Predatory Aggression

Unlike most of the other forms, predatory aggression is largely endogenously generated and accompanied by positive affect (even though the concurrent energizing contributions of hunger may be aversive), and I will argue, contrary to traditional wisdom, that hunting largely emerges from the SEEKING system discussed in the previous chapter.

If, as many scientists used to believe, aggression is largely a learned response rather than an intrinsic potential of the nervous system (e.g., see the contribution by John Paul Scott in the Suggested Readings), it would be unlikely that localized ESB could evoke attack behaviors. However, since Walter Hess’s work in the 1930s (see “Afterthought,” Chapter 4), it has been clear that rage can be precipitously provoked by ESB administered to specific brain areas.

As mentioned at the outset of this chapter, at present three distinct kinds of aggression can be aroused by applying ESB to slightly different brain zones: predatory aggression, angry, ragelike aggression, and perhaps intermale aggression, even though the last may also have strong components of the other two.

 Blame Orienting

Although some electrode sites, especially those low in the brain stem, may only activate motor-pattern generators with no accompanying affective experience, most animals are truly enraged by the ESB. They readily direct their anger to the most salient potential threat in their environment.

For instance, maternal and fear-induced aggression may reflect a convergence of inputs onto an affective attack or RAGE system. On the other hand, intermale, territorial, and sex-related aggression may have some common influence on the system that elaborates intermale fighting, whereas instrumental and predatory aggression may largely arise from the quiet-biting attack systems.

To the best of our knowledge, the two response patterns are simply two distinct behavioral expressions of SEEKING tendencies that arise from homologous systems in the brains of different species.

This does not mean that anger must necessarily be considered a wholly negative emotion. As mentioned, if the energized behavior of rage produces the desired changes in the environment, then it is rapidly mixed or associated with positive emotional feelings.

 Blaming Living Targets

Apparently, during anger, the type of available target is not as important as the fact that there is a living target upon which to vent one’s rage. Yet as one does these types of ESB manipulations in more complex creatures such as monkeys, the aroused animals tend to vent their rage on more submissive animals and avoid confronting more dominant ones.

The core of the RAGE system runs from medial amygdaloid areas downward, largely via the stria terminalis to the medial hypothalamus, and from there to specific locations within the PAG of the midbrain. This system is organized hierarchically (Figure 10.4), meaning that aggression evoked from the highest areas in the amygdala is critically dependent on the lower regions, while aggression from lower sites does not depend critically on the integrity of the higher areas.

 Angry Social Cues

Another set of inputs comes from the orbitoinsular cortex, especially the insular area, where a multitude of senses converge, especially ones related to pain and perhaps hearing. These areas presumably code the affective content of certain irritations, including vocalizations, and may give specific sounds direct access to RAGE circuitry. For instance, it is not an uncommon human experience that an angry tone of voice directed at you activates your own anger in return.

In short, ESB-induced quiet-biting attack could be obtained readily only from those animals that already exhibited some predisposition to attack. Accordingly, it seems that quiet-biting attack is simply one behavioral product of the SEEKING system. Even though this behavior has been extensively studied within the context of aggression, from the animal’s point of view, there is no apparent anger involved in this food-seeking response.

Another fascinating aspect of brain stimulation is that it provokes a predatory temperament only on the side of the brain that is stimulated directly, and this is reflected in the sensitization of the corresponding visual fields. Specifically, ESB applied to the right side of the brain makes an animal exhibit predatory aggression in its left visual field but not in the right (please note that information from the right visual field is transmitted to the left cerebral hemisphere because of the way the optic nerves cross in the optic chiasm).

In nearly all mammalian species, males fight more than females. In neural terms, this is the case because males possess more active aggression circuits, at least those types of aggression circuits that were evolutionarily designed to assure reproductive success. ...In virtually all mammals, male sexuality requires an assertive attitude, so that male sexuality and aggressiveness normally go together.

Although there is no longer much dispute that, in most natural circumstances, males are more aggressive than females (with a few exceptions, such as spotted hyenas), the brain mechanisms for this difference have only recently been revealed. Testosterone has powerful effects on the expression of several brain neurochemical systems.

Testosterone sustains the genetic expression of AVP in a large number of these circuits. Accordingly, males have more extensive vasopressinergic circuits than females.63 When male rats are castrated, AVP is markedly reduced in approximately half of their vasopressinergic circuits. This is paralleled by a decline in both sexuality and aggressiveness.64 If one replaces testosterone directly into the brain via microinjections into the appropriate hypothalamic tissues, these behavioral tendencies return. Several experiments have now directly manipulated the AVP systems, revealing that elevating AVP levels by direct central administration increases intermale aggression in rats.65 In hamsters, centrally administered AVP markedly increases territorial marking behavior, even in the absence of other males.66 If one places an AVP receptor antagonist into the brain, both of these behavioral tendencies are markedly reduced.67 Thus, it would seem that AVP is certainly one factor that promotes intermale aggression; as we will see in Chapter 12, it is also a powerful factor in promoting male sexuality and the formation of social memories. Thus, we can speculate that a molecule such as AVP that can facilitate intermale aggression may only do so because it increases a more generalized male tendency such as behavioral persistence—the relentless and single-minded pursuit of a goal.

As with any emotional system, a great deal of aggressive behavior is learned. Animals can be trained to be more aggressive or more passive. They can be trained to be winners or losers.70 However, it is remarkable how the hormones that promote intermale aggression also provide feedback and reinforce the learning of status. One series of recent findings has shown that victory in a variety of forms leads to increased secretion of testosterone in male animals as well as humans. In humans, such victories as the completion of law or medical school or military training increase plasma testosterone levels.71 Victory on the tennis court can have the same effect.72 To what extent these hormone changes help reinforce future assertive behavior remains to be evaluated, but it would come as no surprise if the neurophysiological solidification of assertiveness was the end result.
Of course, many antiaggressive factors also influence the brain. The “female hormones” estrogen and progesterone have been found to exert antiaggressive effects,73 and it is known that the pleasures of touch and sexuality can inhibit certain types of aggressive tendencies.74 Perhaps the most striking example of inhibition has been found with infanticide, a form of sex-related aggression.75 Males of many species will harm young animals already present in a new territory to which they wish to lay claim. ...At the same time, males should have natural evolutionarily derived inhibitions against harming their own offspring.

Although it has not been demonstrated which brain changes register this type of memory that promotes peaceful coexistence, a reasonable candidate is the gradual induction of oxytocin in the brain. This hormone, which is more prevalent in females than males (see Chapter 12), promotes nurturant behavior (see Chapter 13). Not only is it known to be an effective antiaggressive agent,77 but it can be increased in the brains of male rodents by preceding sexual activity (see Chapter 12).

In general, reduced brain serotonin activity also tends to increase impulsive and acting-out forms of behavior in humans.

Although affective neuroscience research can provide us with a substantive knowledge of the experience of anger, it cannot explicate the cultural, environmental, and cognitive causes of aggression. In humans, it is usually the appraisal of events that triggers anger; obviously, many values upon which appraisals are premised are culturally learned in humans.

 Chapter 11

Contrary to traditional thinking on the topic, which taught that fears simply reflect learned anticipation of harmful events, it now appears that the potential for fear is a genetically ingrained function of the nervous system. This should come as no surprise. An organism’s ability to perceive and anticipate dangers was of such obvious importance during evolution that it was not simply left to the vagaries of individual learning. Even though learning is essential for animals to utilize their fear systems effectively in the real world, learning does not create fear by pasting together a variety of external experiences. Evolution created several coherently operating neural systems that help orchestrate and coordinate perceptual, behavioral, and physiological changes that promote survival in the face of danger. The emotional experience of fear appears to arise from a conjunction of neural processes that prompt animals to hide (freeze) if danger is distant or inescapable, or to flee when danger is close but can be avoided.

[Animal] investigations indicate that the capacity to experience fear, along with fear-typical patterns of autonomic and behavioral arousal, emerges primarily from a FEAR circuit that courses between the central amygdala and the periaqueductal gray of the midbrain. Fear behaviors can be evoked by artificially activating this circuit, and conditioned fears can be developed by pairing neutral stimuli with unconditional stimuli, such as electric shock, that can arouse this emotional system. In other words, conditioned fears emerge by neutral stimuli gaining access to this system via learning. Higher cortical processes are not necessary for the activation of learned fears, although those processes refine the types of perceptions that can instigate fear.

It is likely that the affective impact of both experiences emerges ultimately from the differential arousal of one and the same brain system—a coherently operating FEAR circuit that produces terror when precipitously aroused and chronic anxiety during milder, more sustained arousal. The FEAR system can be activated by various world events, as well as by internal ones. External stimuli that have consistently threatened the survival of a species during evolutionary history often develop the ability to unconditionally arouse brain fear systems. For instance, laboratory rats exhibit fear responses (increased freezing and inhibition of other motivated behaviors) to the smell of cats and other predators (see Figure 1.1), even though they have never encountered such creatures in their lives, having grown up in the safety of a controlled laboratory setting (for more on the underlying neural mechanisms, see the “Afterthought” of this chapter).
In addition to such inborn tendencies, a variety of specific anxieties can be acquired during the life span of each individual. These are usually triggered by specific external events that have been paired with pain or other threatening stimuli, but it is important to recall that feelings of fear can also emerge simply from the internal dynamics of the brain (so-called free-floating anxieties). Internal stimuli that can arouse the FEAR system range from irritative epileptic foci in the limbic system to conscious as well as unconscious memories of past occurrences.

Even though many higher cortical perceptions sustained and exacerbated your fears, to the best of our knowledge, the resulting chronic hyperemotional state is created by deep subcortical networks that can become sensitized and can operate independently of your higher cognitive faculties. For this reason, long-lasting fears and anxieties can lead to chronic psychological distress that does not always respond well to standard cognitive therapies.

Experientially, fear is an aversive state of the nervous system, characterized by apprehensive worry, general nervousness, and tension, which tells creatures that their safety is threatened.

However, there are distinct sites in the brain where electrical stimulation will provoke a full fear response in all mammalian species, and these are locations where the executive system for FEAR is concentrated. These are in the lateral and central zones of the amygdala, the anterior and medial hypothalamus, and, most clearly (and at the lowest current levels), within specific PAG areas of the midbrain.

Although pain is an especially effective stimulus for creating fear and generating learned fears, it does not constitute fear itself. To the best of our present knowledge, fear—the subjective experience of dread, along with the characteristic set of bodily changes—emerges from the aforementioned circuit, which interdigitates extensively with the RAGE circuit. In the amygdala, however, the two systems are fairly clearly segregated, with FEAR being more lateral and RAGE more medial. As mentioned, the FEAR circuit courses from the lateral and central nuclei of the amygdala, through the ventral-anterior and medial hypothalamic areas, down to the mesencephalic PAG (Figure 11.1). Freezing, as well as flight behavior and the autonomic indices of fear (e.g., increased heart rate and eliminative behavior), can be evoked along the whole trajectory of this system.

It makes good evolutionary sense for FEAR and RAGE circuits to be intimately related, for one of the functions of anger is to provoke fear in competitors, and one of the functions of fear is to reduce the impact of angry behaviors from threatening opponents. Although it has not been empirically demonstrated, it is reasonable to suppose that at low levels of arousal, the two systems are mutually inhibitory (see Figure 3.5). At very sudden or intense levels of arousal, however, both the fear response and the rage response may be concurrently aroused....
Since mild fear is characterized largely by behavioral inhibition components, while intense fear is commonly characterized by active flight, it is important to consider how these diametrically different response tendencies might be elaborated by the FEAR system. By carefully following the behavioral responses evoked by different intensities of stimulation, it has become clear that one can promote freezing during mild arousal of this system and flight at higher stimulation intensities (Figure 11.2).

However, it is now clear that a reduction of brain serotonin makes animals more manic and impulsive in general, with a very broad pattern of behavioral disinhibition in situations that entail anxiety as well as those that do not. ... Rather, it is clear that the serotonin system modulates the intensity of fear, but to no greater extent than it modulates other negative emotions. In fact, most of the available data is still consistent with the alternative conclusion that an overall increase of serotonin activity decreases anxiety and produces feelings of relaxation.

In other words, anticipatory anxiety and panic were modulated by different neurochemical systems. ...
Recently, a strong case has been put forward claiming that panic attacks emerge from primitive suffocation-alarm systems of the brain, which may be closely coupled with separation-distress systems. Thus, although PANIC and FEAR systems can be distinguished in the brain (also see Chapter 14), it is to be expected that they can also operate synergistically: Chronic anxiety can increase the incidence of panic attacks, and panic attacks can lead to chronic anxiety.

Brain-stimulation studies have long suggested that a coherently operating FEAR system exists in the brain. As mentioned previously, it extends from the temporal lobe (from central and lateral areas of the amygdala) through the anterior and medial hypothalamus to the lower brain stem (through the periventricular gray substance of the diencephalon and mesencephalon) and then down to specific autonomic and behavioral output components of the lower brain stem and spinal cord, which control the physiological symptoms of fear (including increases in heart rate, blood pressure, the startle response, elimination, and perspiration; for a summary see Figure 11.1). A growing consensus is emerging that this neural system mediates a fundamental form of unconditional fear. Minor tranquilizers exert part of their antianxiety effect by reducing arousal of this brain system.

When this system is activated by electrical stimulation of the brain (ESB), animals exhibit a variety of fearlike behaviors, ranging from an initial freezing response at low current levels to an increasingly precipitous flight response at higher current intensities. These, of course, reflect the types of fear responses animals normally exhibit when dangers are either far or close. In other words, the responses evoked artificially by ESB look very similar to the behavior of animals that have either noticed a predator at a distance or are being pursued by one.

Even though animals exhibit flight when this system is stimulated, they do not readily learn to avoid the brain stimulation that evoked the fearful behaviors. In other words, a neutral cue predicting the onset of ESB in the FEAR system does not readily become a conditional source of fear that is sufficient to motivate the learning of discrete avoidance responses.

First, all animals readily learn to escape such stimulation, implying that this type of ESB is highly aversive. The more closely the requisite learned response resembles the ESB-induced flight, the more rapidly the animal learns. Thus, the act of running away is learned more rapidly than a lever-press response.
If given the opportunity, animals will avoid environments where they have received such stimulation in the past, and if no avenue of escape is provided, they will freeze as if in the presence of a predator.

Animals readily learn to escape from and avoid places where they have been hurt. Current evidence suggests that pain and fear systems can be dissociated even though they interact strongly at various locations within the neuroaxis (including the lowest reaches in the PAG, as well as the highest reaches in the amygdala). ... Thus, even though pain systems do send inputs into areas of the brain that mediate fear (especially at the PAG of the mesencephalon), electrical activation of the FEAR system does not appear to readily evoke the sensation of pain in either humans or animals.
However, it is also clear that the FEAR system does control pain sensitivity. It is commonly observed that animals and humans do not focus on their bodily injuries when they are scared,45 and fear-induced analgesia emerges, at least in part, from arousal of pain-inhibition pathways such as serotonin and endogenous opioids, near the PAG of the mesencephalon.

The FEAR system contains certain intrinsic sensitivities, in that it responds unconditionally to pain and the smell of predators and other intrinsically scary stimuli, but it can also establish new input components that function through learning to inform the organism about cues that predict threats. Some environmental circumstances lead to rapid conditioning, presumably because certain perceptions have ready access to the FEAR system, while neutral stimuli take longer to condition. ... In other words, the brain is predisposed to associate fear with the potentially threatening configuration of anger more readily than with a pleasant face. ... There are bound to be several preferential input channels to the FEAR system, reflecting the different intrinsic fears of different species. Thus, humans readily exhibit fears of dark places, high places, approaching strangers (especially those with angry faces), and sudden sounds, as well as snakes and spiders.49 Rats are especially apt to fear well-illuminated areas, open spaces, and the smell of cats and other potential predators. But completely neutral stimuli can also access the FEAR system of the brain. During the past few years, great progress has been made in unraveling the manner in which this system becomes classically conditioned when neutral cues are paired with shock.
One of the first breakthroughs in the field was the finding that conditioned fears access the FEAR system at the central nucleus of the amygdala.50 When this area is lesioned on both sides of the brain, animals no longer exhibit increased heart rates to stimuli they had learned to fear.51 It is now becoming clear that the central nucleus is one major brain area where conditional synaptic control of fear is created.

In any event, the preceding results affirm that emotional learning can occur without the intervention of the highest reaches of the cognitive brain. There are direct anatomical entry points from the thalamus into the relevant amygdaloid circuits, but it is clear that the more indirect cortical and hippocampal connections also provide information about external threats. For instance, the hippocampus informs animals about threatening aspects of their spatial environments, but it does not process discrete fear stimuli as does the amygdala.60 Conditioning, as well as affective experience, can probably also be elaborated at lower levels of the fear circuit (i.e., at hypothalamic and mesencephalic levels), but such important issues remain to be empirically evaluated.

In addition to real-world threats and dangers, ESB along the FEAR circuit generates powerful fear responses and the corresponding negative affective states in experimental animals and humans. Pharmacological and surgical dampening of activity along this system can make both animals and humans placid. In short, many expressions of fear emerge directly from this neural system, and it is only a matter of time before the many subjective feelings of fears will be understood with the tools of modern neuroscience.

In essence, the brain’s capacity for fear is an evolved process that arises ultimately from internal neural causes rather than simply from the terrors of the environment.

 Chapter 12

...the female brain coordinates the use of both cerebral hemispheres more effectively than does the male brain.

The primordial plan for both female and male fetuses, in mammals but not in birds, is initially feminine. ...To be masculinized means that certain areas of the brain, especially specific nuclear groups in the anterior hypothalamus, grow larger in males than in females, while other areas remain smaller, such as the corpus callosum, which connects the two cerebral hemispheres. These brain organizational effects of early hormone secretions go a long way toward explaining some homosexual tendencies, for the hormones that ultimately trigger the organization of the male brain (testosterone aromatized to estrogen) are distinct from those that trigger the organization of the male body (testosterone converted to dihydrotestosterone, or DHT, by 5α-reductase).

However, mammals also exhibit major brain functional differences between the sexes. For instance, preoptic area damage has more deleterious effects on male sexual behavior than on female behavior, while ventromedial hypothalamic damage has the opposite effect, compromising female urges more than those of males. These brain areas are organized differently in males and females. To have a male or female brain means many things, but among the best-established effects are the higher prevalence of arginine-vasopressin (AVP) circuits in males and more extensive oxytocin circuits in females.

Many surveys of human mate preferences indicate that females are seeking companions who are powerful and willing to invest resources in their behalf, whereas males are swayed more by youth and beauty, namely, external indicators of reproductive fitness. (Buss 1994 "The Strategies of Human Mating"; Buss 1994 The Evolution of Desire: Strategies of Human Mating)

The biological constraints that all mammals share contain no prescription for what human sexual behavior should be. As always, in the subcortical reaches of the brain, the evidence can only tell us what is; it does not inform us about what should or could be, especially when it comes to creatures as complex as humans.

In many mammals, the vigor of male sexuality and male assertiveness (i.e., social dominance) tend to go together, and we are finally beginning to understand the underlying neural conjunctions. The fact that male sexuality and aggression interact to a substantial extent in subcortical areas of the brain is now a certainty (see Chapter 10).

To approximate the biological nature of things, the first tenet we need to accept is that male and female sexualities are as differently organized in male and female brains as they are in bodies. Although learning mechanisms are of obvious importance in generating the details of gender identity, the different sexes value substantially different things because of the distinct types of brain mechanisms and psycho-biological values with which they are endowed. As already mentioned, human males are enticed by youthful beauty, while females are enticed by resource commitment. We also see this in other primate societies. Male chimpanzees usually fight over meat and sexual issues and also during social reunions, while females exhibit aggression largely in the context of seeking protection, competing for plant foods, and protection of the young.
To some extent, especially in humans, the different gender expectations are culturally biased, but there are many psychobiological differences that are not simply a matter of choice or learning. For instance, males are more aggressive and power-oriented, while females are more nurturant and socially motivated. Indeed, recent brain metabolic evidence in humans indicates that temporal lobe areas (where aggression circuitry is concentrated) are more active in males, while cingulate areas (where nurturance and other social emotional circuitries are concentrated) are more active in females.16 Such natural gender differences (at least at a population level) should no longer be a matter of debate, for the empirical facts seem overwhelming.

Oxytocin has more effect on female sexual and social behavior, while vasopressin (which differs from oxytocin by only two amino acids) retains the ability to govern male sexuality. ... Vasopressin, which is more abundant in the male brain, is especially important in the mediation of many aspects of male sexual persistence (including courtship, territorial marking, and intermale aggression). Oxytocin, which is more abundant in female brains, helps mediate female social and sexual responsivity (especially the tendency of female rodents when mounted to exhibit lordosis postures, a characteristic, arch-backed, female receptivity reflex).19 It is even more remarkable that after the birth of the young, these same synaptic modulators encourage parents, especially the mothers but at times also the fathers, to take care of their offspring (see Chapter 13).
...Vasopressin systems may help energize some of the more aggressive aspects of maternal behavior (i.e., protecting the young from harm); conversely, oxytocin systems may sustain some of the gentler aspects of male behavior (e.g., the tendency of fathers to be nonaggressive and supportive toward their offspring).20 It cannot be emphasized too much that brain oxytocin is not completely reserved for female functions. It also has some role in governing male sexuality, just as vasopressin may have some role in females (i.e., reducing sexual readiness and increasing maternal aggressiveness).

The hormonal patterns that are set in place during the organizational phase of fetal development help “expose” the imprint of maleness or femaleness on maturing brain circuits, as well as on bodily appearance. The hormones secreted at the onset of puberty eventually “develop” the exposed “negative,” thereby activating the latent male or female sexual proclivities that have remained comparatively dormant within brain circuits since infancy.

Females [exposed to too much estrogen during development] will preferentially exhibit male-typical behaviors at maturity, but only if their brains are exposed to the activational effects of testosterone at that time. Indeed, in humans, tomboyishness in females has been promoted by maternal injections of diethylstilbestrol (DES), an estrogenic hormone that was given to pregnant mothers during the second trimester to prevent miscarriages in the 1940s and 1950s.

Although socialization certainly influences the sexual roles individuals choose, it now appears less crucial than has been widely believed in the arena of basic sexual feelings. For instance, the Dominican XY males who lacked 5-α-reductase did not experience extreme difficulty in reorienting their lives as males following puberty, even though they had been reared as girls. In contrast, boys who have lost their genitalia early in life and have been reared as girls throughout their childhood have been found to experience considerable emotional distress and confusion at puberty when they are expected to behave like women.

The largest subcortical differences have been found in the anatomy and chemistry of the medial preoptic area (POA), where males in practically all species studied have significantly larger neuronal densities than females. ...In females, many neurons [the SDN-POA] die during fetal development for lack of testosterone, or more precisely its product estrogen, which is a powerful growth factor for these neurons.

In sexually experienced rats, this area [the POA] is more important for the generation of sexual behavior than sociosexual motivation. ...Neurophysiological studies in primates indicate strong neural arousal in the POA not only when animals are copulating but also when males are approaching the subject of their desire. Comparable effects are not seen when they approach other objects of desire, such as a bunch of bananas!

When a pregnant rat is exposed to any of a variety of stressors during the last trimester (third week) of the three-week gestation period, many of the male offspring exhibit gender ambiguity when they reach puberty. Commonly, the experimental stress imposed on such mothers has consisted of prolonged immobilization, with continuous exposure to bright light, which rats dislike and which also generates thermoregulatory discomfort. However, many other stressors, such as foot shock or overcrowding, have also been used with comparable results. In a normal litter from unstressed mothers, approximately 80% of the males become “studs” at puberty, while the rest remain asexual “duds,” which exhibit little male- or female-typical sexual behavior. Among the male pups of stressed mothers, however, only about 20% become “studs,” while about 60% either are bisexual (exhibiting male behavior with a highly receptive female, and female behavior in response to a “stud” male) or else exhibit exclusively female sex behaviors (i.e., they exhibit lordosis, the characteristic female-specific receptivity pattern, when mounted by a sexually aroused male). The remaining 20% are asexual, as in unstressed litters.
...
...female offspring of stressed mothers exhibit weaker maternal tendencies than those from nonstressed mothers—just the converse of the pattern seen in males, who tend to become more nurturant.

In sum, even though environmental effects clearly modify one’s self-perceptions, the sources of gender identity, as genetic sex itself, are heavily rooted in biology. Although it would be foolish to conclude that sexual preferences are completely controlled by nature, we can no longer discount innate biological influences.

In general, experienced male rats housed alone in their cages are always ready for a little sex. Females, on the other hand, are not. Female rats typically have four-day sexual (estrus) cycles, and only for several hours on the day of estrus are they willing to participate in copulation. Nature has assured, for most species, that sexual arousal in females is tightly coordinated with peak fertility.

...human females exhibit a “concealed ovulation” with no clear “estrus cycle”...This means that sexual urges and the likelihood of fertilization have been dissociated to a substantial extent in our species, which may help promote male investment and pair-bonding with individual women. In other words, a human male cannot identify which female is ovulating by any external sign. Hence, for reproductive success, he needs to be more attentive to one female’s needs for longer periods of time than is characteristic of most mammals.

The sexually aroused female rat also has a variety of active behaviors to attract males. These “flirtatious” appetitive or proceptive behaviors appear designed to capture the attention of a male and entice him to pursuit. The most evident behaviors in the rat are repeatedly running toward and away from the male, or past him in a hopping, darting fashion with the head wiggling and many 50 KHz vocalizations. Many of these behaviors also characterize play solicitation behaviors, which precede rough-and-tumble juvenile wrestling (see Chapter 15).

It may also be worth noting that starved animals are much less likely to mate than are well-fed ones, and the linkage between energy balance and mating readiness may be neurally negotiated directly within the VMH. Obviously, it is unwise to seek reproduction when energy resources are low, and nature has assured that this is unlikely to happen.

In contrast, human females are more willing than most other mammals to indulge in sex independently of their hormonal status, but it is also clear that better studies concerning the sexual-emotional motivation of women need to be done before we exclude the importance of hormonal fluctuations. At best, human females exhibit only a modest trend for increased receptivity during ovulation.

The proximity of sexual and aggression control circuits in the male brain should also lead us to pause and wonder about possible functional relationships.
In a certain sense, this is the male dilemma: The hormonal stimuli that promote sexuality also increase certain types of aggressiveness.76 If male animals are castrated, both their sexual ardor and their pugnacity diminish gradually, as do levels of AVP in approximately half the neural systems of the brain. Although sexuality can continue without brain AVP, it is sluggish, lacking the high level of persistence characteristic of sexually aroused males. While castration leads to a gradual decrease of sexuality in normal males, it leads to a rapid cessation of sexuality in genetically impaired animals that have little vasopressin in their brains to begin with (e.g., rats of the Brattleboro strain).
...Indeed, when AVP is artificially increased in the female brain, sexual receptivity plummets. Perhaps the presence of this male sex factor impairs female sexuality by making the females more aggressive (see Chapter 10).

By contrast, the female brain contains more oxytocin neurons than the male brain, and the genetic manufacture of oxytocin is under the control of the ovarian hormone estrogen.80 The role of this neuropeptide in sexuality is not as lopsided as that of vasopressin in the male brain. Administration of oxytocin directly into the brain can increase both male and female sexuality, but seemingly in different ways. In males, oxytocin promotes erectile capacity, and it is released into the circulation in large amounts at orgasm (Figure 12.6). Unfortunately, no comparable data appear to be available for females. In any event, at present, brain oxytocin release is a key candidate for being a promoter of orgasmic pleasure and hence one of the mediators of behavioral inhibition commonly seen in males following copulation.
There is a certain beauty in the fact that oxytocin, a predominantly female neuromodulator, is an especially important player in the terminal orgasmic components of male sexual behavior. In that role it may allow the sexes to better understand each other. ...While oxytocin does modulate the orgasmic phase of male sexual activity, in females it appears to be important for both the courting and copulatory phases. In less clinical terms, it activates female flirtatiousness as well as sexual ardor.

It has long been known that [the ventromedial nucleus of the hypothalamus] is uniquely important for normal female receptivity. Damage can seriously impair female sexual responsivity while having little effect on male sexuality. ...The sex hormones that prepare the body for fertilization also dramatically change neurochemical sensitivities in this part of the brain.

For instance, one especially intriguing finding is that a male’s “jealous” attachment to a female may be dependent on the fact that AVP was active in his brain during sexual activity. At least in prairie voles, the only species studied so far, sexual activity can increase the likelihood that a male will attack potential interlopers. Males that are allowed to copulate will become aggressive toward other males that enter their territory. However, if an AVP antagonist is placed into the brain just prior to the sexual activity, these field mice do not develop such a jealous attitude. On the other hand, if one simply puts AVP into the brain of a male in the presence of a female, with no sexual activity allowed, the males still begin to treat other males in threatening ways.88 If one is willing to generalize from these behavioral results to human feelings, one might hypothesize that tendencies for sexual jealousy are promoted in the male brain by the release of AVP during sexual activity.

Such experiments have clearly indicated that opiate blockade is more effective than dopamine blockade in attenuating sexual reward in males.

One important line of evidence that supports the idea that male and female eroticism have converged in humans is the finding that sexual desire in females is more dependent on adrenal testosterone than in other mammals,92 whose receptivity relies more critically on ovarian estrogen and progesterone.

Although there is considerable variability from one species of bird to the next, the most common theme is that birdsong is not completely formed within the genetically connected components of their song circuits; rather, in most species, there is only a rudimentary form of the species-characteristic “score” embedded within the genetically dictated connections of those circuits. To become complete, circuit functions need to be optimized through learning, and the birds need to be able to hear their own fledgling attempts at song production. Without early exposure to their own song, the males of most passerine species (i.e., songbirds) will exhibit only a few fragments of their ancestral tunes.95 In the absence of any better role model, some species are able to approximate the songs of other species heard during their youth, but most will fully perfect only the song of their own species.

Human courtship and sexual styles are obviously learned. The passions that accompany them are not. It seems likely that biological factors are as influential in the hidden desires of the human heart as they are in the birdsong of springtime.

Animals have been found to exhibit remarkably consistent hormonal fluctuations as a function of their social successes, and similar changes are also evident in humans. As mentioned in Chapter 10, the winners of social encounters typically exhibit elevations in circulating testosterone, while losers exhibit declines.

(1) Young females, including humans, typically become sexually mature more rapidly when strange males enter their environments. (2) Social stimulation can modify levels of bodily enzymes controlling the manufacture and processing of sex steroids. (3) Groups of female primates, as well as wolves and other species, exert physiological influences over each other to control which animals will reproduce in the group (perhaps via olfactory cues). (4) Finally, we are beginning to find that the olfactory senses of human beings may also be acutely sensitized to certain smells that can synchronize sexual cycles and hence may coordinate sociosexual activities.

 Chapter 13

The ongoing physiological changes that prepare the body for birth also prepare the mother’s brain for nurturance. In most animals this includes her role as the primary caregiver. Males can be trained to exhibit a high level of nurturance, but their care is rarely as natural or as intense a motive as it is for the mother. Only in species where male participation is absolutely essential for offspring survival, as in some birds and perhaps in humans, where the child is helpless for longer than any other animal, can nurturant behavior be as vigorous in males as it is in females.

The nurturant circuits in the mother’s brain and care-soliciting circuits in infants are closely intermeshed with those that control sexuality in limbic areas of the brain. This confluence lends modest support to controversial and widely debated Freudian notions of infantile sexuality and the possible relations between maternal love and female sexuality.

Nurturance circuits can lead to the rapid learning of maternal behaviors, which then become permanent parts of a mother’s behavioral repertoire. Males can also learn nurturant behaviors, and it is intriguing that sexual activity can strengthen antiaggressive, caregiving substrates in male brains.

For humans, the rearing of a child is as much an economic question as an emotional one, and economic concerns often prevail. Antecedents of this are evident even in some lower species, where mothers kill some of their weaker pups. When environmental resources are scarce, this practice can increase the probability of success for the surviving offspring.

Prey species are typically born rather mobile, so they can run away from predatory dangers soon after birth. They also tend to live in herds where the young can easily get separated from parents. Thus, out of sheer necessity, mothers and infants must bond rapidly. Predators, on the other hand, are typically born relatively immature, and the bonding process, at least from viewpoint of the offspring, can be extended across longer periods without compromising their chances of survival.

Some animals, such as infant rats, bond as much to their nest sites as to their mothers.7 Likewise, rat mothers readily accept strange pups into their nests and begin to provide care without much fussing or aggression. Sheep and other ungulates, on the other hand, will reject others’ young.

At present, brain oxytocin, opioids, and prolactin systems appear to be the key participants in these subtle feelings that we humans call acceptance, nurturance, and love—the feelings of social solidarity and warmth.

I use the term CARE circuits to acknowledge the existence of intrinsic brain systems that promote nurturant behaviors of mothers, and occasionally fathers, toward their offspring. In rats, full maternal behavior consists of building nests, gathering all dispersed pups together, hovering over them to provide warmth, and, in the presence of lactation, sustaining pups through nursing. In most species, mothers are more adept at these behaviors than fathers, presumably because of the more vigorous CARE systems in their brains, but this is not to suggest that males cannot exhibit nurturance.

Not surprisingly, if we dwell on the matter, maternal urges probably emerged (i.e., were exaptations) from a subset of subcortical systems that initially governed female sexual urges. It would also have been reasonable to couple parental emotions to the preexisting psychobehavioral systems that encourage individuals to come together for mating. Thus, maternal nurturance and social bonding may have emerged from evolutionary tinkering with preexisting processes, rather than through totally new forms of brain “engineering.”

As François Jacob, the Nobel Prize-winning molecular biologist, put it: “Natural selection … works like a tinkerer … who does not know exactly what he is going to produce but uses whatever he finds around him … to produce some kind of workable object…. Evolution makes a wing from a leg or a part of an ear from a piece of jaw…. Natural selection … does not produce novelties from scratch. It works on what already exists.”

As mentioned in the previous chapter, vasotocin is an ancient brain molecule that controls sexual urges in reptiles. This same molecule, the precursor of mammalian oxytocin, also helps deliver reptilian young into the world. When a sea turtle, after thousands of miles of migration, lands on its ancestral beach and begins to dig its nest, an ancient birthing system comes into action.14 The hormone vasotocin is secreted from the posterior pituitary to facilitate the delivery of the young. Vasotocin levels in the mother turtle’s blood begin to increase as she lands on the beach, rise further as she digs a pit large enough to receive scores of eggs, and reach even higher levels as she deposits one egg after the other. With her labors finished, she covers the eggs, while circulating vasotocin diminishes to insignificant levels (Figure 13.2). Her maternal responsibilities fulfilled, she departs on another long sea journey. Weeks later, the newly hatched turtles enter the world and scurry independently to the sea without the watchful, caring eyes of mother to guide or protect them.
In mammals, the ancient molecules that control reptilian sexuality and egg laying evolved into the oxytocin and arginine-vasopressin (AVP) social circuits of the brain (see Figures 6.7 and 12.2). As discussed in the previous chapter, oxytocin came to prevail in female sexual behavior, and AVP prevails in that of males. Now we also know that oxytocin—the hormone that helps deliver mammalian babies by promoting uterine contractions and helps feed them by triggering milk letdown from mammary tissues—also serves to facilitate maternal moods and related action tendencies in the brains of new mothers.

These hormonal changes heralding imminent birth also prepare the mother to exhibit maternal urges before the actual arrival of the infant(s). Human mothers commonly exhibit a compulsive flurry of house preparation several days before the baby is due, and rat mothers begin to build nests and become substantially more eager to interact with baby rats. Such tendencies are common in many species and are especially clear if the mother has given birth before.

Finally, and quite perplexingly, oxytocin is effective only if animals have been habituated to test chambers for a few hours but not if they have been fully habituated for a day or more. This may mean that if animals already have a reasonably well-established place attachment, they have difficulty forming new social attachments.

It presently seems likely that part of the gratification derived from the primal act of nursing emerges from the concurrent release of oxytocin and opioids within the limbic system, as well as other chemistries that remain to be identified. While oxytocin may be especially important in the initial triggering of maternal behavior, prolactin, opioids, and social learning are important in sustaining it once the behavior pattern has developed.

It should be emphasized that well-established maternal behavior no longer requires brain oxytocin arousal; oxytocin blockade impairs maternal behavior only if administered to mothers during the birth of their first litter of pups. In animals that have been allowed to exhibit maternal behavior for several days, oxytocin antagonists have no outward effect on maternal competence. In other words, they cannot block previous social learning.

Oxytocin only works when supplemented with other social stimuli. By comparison, it is easy to obtain simple reward effects with opiates and psychostimulants.

It is especially noteworthy that neural circuitry for maternal behavior (and estrogen-responsive populations of oxytocin cells) are situated within the dorsal preoptic area (POA) just above the brain areas that elaborate male sexuality. These cells probably control nurturance in both males and females, but there are more of them in females, partly because of the inductive effect of estrogen.

It has been established that the oxytocinergic synapses that terminate on dopamine cells of the VTA do, in fact, promote maternal behavior. Oxytocin injections into the VTA can induce maternal behavior, whereas comparable injections are not effective in amygdala, septum, or POA.

If this oxytocin-VTA interface is relatively nonspecific, the additional oxytocin influences, perhaps lower in the brain stem, may be essential for engaging specific motivational circuits for maternal behavior, such as sensitization of affective responses to specific forms of somatosensory stimulation such as suckling. We do not yet know where those circuits are situated, although there are some clues.45 Alternatively, it is possible that oxytocin input to the VTA can intrinsically code a subtype of appetitive eagerness that is specifically directed toward expressions of nurturant behaviors.

As John Bowlby poignantly documented in a series of books,49 a child that never had a secure base during childhood may spend the rest of its life with insecurities and emotional difficulties.

Indeed, opiate addiction in humans is most common in environments where social isolation and alienation are endemic. Investigators have been able to increase opiate consumption in experimental animals simply by separating them from companionship.

Considering the importance of oxytocin for maternal behavior, it has also been of great interest to determine whether the molecule modulates negative emotions that arise from separation. Indeed, as discussed in detail in Chapter 14 oxytocin and vasotocin have turned out to be extremely powerful inhibitors of the separation call in various species, affirming that social comfort is produced by the same brain chemistries that help mediate maternal and sexual behaviors.
Moreover, it is noteworthy that the oxytocin molecule has special properties to increase the sensitivity of brain opioid systems. Organisms typically exhibit tolerance to opiates, as in the case of addicts who must administer ever-increasing amounts to obtain the same psychological response. Oxytocin can inhibit the development of this tolerance. Perhaps the secretion of oxytocin in nursing mothers blocks tolerance to opioid reward, and thus provides a dual way for the maternal experience to sustain social pleasures: not only by directly activating oxytocin-based social reward processes but also by sustaining high affective arousal in the brain’s opioid experiences. It would be disastrous if mothers lost their ability to feel intense social gratification from nurturance when children were still quite young.

Male prairie voles, an especially gregarious mouse strain, will choose to spend time with those females in whose company they have experienced elevated levels of AVP.

Animals also prefer to spend more time with other animals in whose presence they have experienced high brain oxytocin and opioid activities.62 Thus, it seems as if friendships are cemented by the same chemical systems that mediate maternal and sexual urges. Perhaps this is one of the primitive emotional reasons we are more likely to help family and friends than strangers (a phenomenon called kin selection by sociobiologists).

In fact, low doses of oxytocin, which are more likely to be in the natural physiological range, also strengthen social memories.65 Thus, the same brain chemistries that facilitate various friendly social and sexual behaviors also help solidify the memories that emerge from those experiences.
It remains a mystery exactly where and how memories promoted by oxytocin are solidified in the brain. Interestingly, however, the hippocampus, which is a key brain area for the consolidation of memories, has high oxytocin and AVP sensitivity.

Generally, rat mothers sequester their offspring in nests and exhibit a great deal of tolerance if their babies are replaced with strangers. They appear to be satisfied as long as some young remain in the nest, for they seem to be attached more to the general concept of having babies in their nests than to their own specific babies, presumably because the appearance of strangers has been a rare event in their evolutionary history. On the other hand, in most herbivores, babies are born motorically precocious, and the mothers must rapidly establish discriminating bonds.

Although all this is true, we should remember that in mammals the social bonding mechanisms are based on learning and are certainly more pervasive than the innate mechanisms for “kin recognition.” We can learn to love other animals.

One of the most intriguing general psychological phenomena related to those discussed here is called the “mere-exposure” effect. If one simply exposes animals to various stimuli, they begin to develop a preference for those stimuli, especially if they have been paired with positive affective experiences.86 This effect is pervasive and applies to all species and most objects that have been studied.87 If one has been exposed to certain foods, one begins to prefer those foods.88 If one has been exposed to certain objects and places, one begins to prefer those objects and places.89 Indeed, place attachment arises from mere exposure, which may have been one of the antecedent processes for social bonding. Much of the mere-exposure effect operates at a subconscious level and may be related to other preconscious evaluative effects of emotional stimuli. For instance, it has been demonstrated that if one simply exposes American students to written Chinese characters they do not understand, some of which are preceded by a brief subliminal presentation of a smiling face, subjects will later prefer those characters as opposed to ones that were shown without affective priming.

 Chapter 14

When [a sea otter mother] dives beneath the dark surface of the water for food, being absent from her infant’s side for many minutes at a stretch, the young otter begins to cry and swim about in an agitated state. If it were not for those calls of distress among the rising and falling waves, young otters might be lost forever. Their security and future are unequivocally linked to the audiovocal thread of attachment that joins them to their mothers. It is the same for all mammals. At the outset, we are utterly dependent creatures whose survival is founded on the quality of our social bonds—one of the remaining great mysteries, and gifts, of nature.

For instance, although young rats exhibit a very short period after separation when they emit separation calls (see Figure 2.1), they show many other long-lasting changes, including decreases in body temperature, sleep, and growth-hormone secretion, along with increases in brain arousal, behavioral reactivity, sucking tendencies, and corticosterone secretion.2 The patterning of these responses is influenced by complex physiological controls, but an understanding of brain emotional changes also will be essential to explain this symptom complex.

There are good reasons to believe that neurochemistries that specifically inhibit the separation-distress or PANIC system also contribute substantially to the processes that create social attachments and dependencies—processes that tonically sustain emotional equilibrium and promote mental and physical health throughout the lifetime of all mammals.
The mammalian brain contains at least one integrated emotional system that mediates the formation of social attachments. The affective components of this system are dichotomous—behaviors and feelings of separation distress on one hand, and those of social reward or contact comfort on the other (Figure 14.1). The existing data suggest that arousability in this system is controlled by multiple sensory and perceptual inputs, and that the evolutionary roots of the system may go back to more primitive control mechanisms such as those elaborating place attachments in reptiles, the basic affective mechanisms of pain, and fundamental creature comforts such as thermoregulation.
One of the key issues for future research will be whether social reward processes exist independently of the neurochemistries that can inhibit separation distress. It is remotely possible that there is no distinct social reward process, since the candidate systems—the opioids, oxytocin, and prolactin—all inhibit separation distress quite well.

Social attachments are probably promoted by the ability of certain interactions (and their attending neurochemistries) to alleviate that mild form of separation distress that we call loneliness.

Brain opioids were the first neurochemistries discovered to powerfully reduce separation distress.

How these attachment tendencies emerge from the fabric of the brain has remained a mystery until recently. Now, work on animal emotionality is beginning to reveal the neuromotivational forces that may mediate such social feelings. An especially promising line of work is emerging from the detailed analysis of one behavioral measure—the vocal “crying” aroused by social isolation in young animals. Some label these “isolation calls,” others refer to them as “distress vocalizations,” and others simply call it “crying” (a label that many behavioristically oriented investigators deem too anthropomorphic). The label is less important than the fact that there is an intrinsic neural system in the brain, here labeled the PANIC system, that mediates this strong emotional response.

Since the infants of all mammalian species remain quite helpless for a variable period of time following birth, they must have strong distress signaling mechanisms to solicit and sustain parental care. Isolation calls, or distress vocalizations (DVs), as they will be called here, are one of the most primitive forms of audiovocal communication (Figure 14.2); the underlying brain mechanisms are probably shared homologously in all mammals, even though there is bound to be substantial variation among different species depending on their socioecological circumstances.

In any event, DVs [distress vocalizations] emerge quite promptly whenever young animals are left alone in strange new places. The proximity of a caretaker is typically sufficient to totally inhibit the calls in both humans and other species (Figure 14.3).14 The home location can also inhibit separation distress to a modest extent, suggesting that separation-distress systems may be evolutionarily related to ancient mechanisms of place attachment.

...the neural systems for separation-induced crying emerged from more primitive distress mechanisms, such as those that mediate pain and feelings of coldness...

In animals, there is evidence to suggest that separation-induced DVs can be distinguished from cries of pain on neuroanatomical and neurochemical bases, as well as via an analysis of sound spectrum characteristics.1

In the presence of adults who have bonded with the young, DVs have the common effect of arousing the attention and typically the caregiving motivations of caretakers.

It is a common assertion that human females are prone to cry more than males. There may be some neurobiological truth to this stereotype. Work on the isolation cries of guinea pigs and chickens indicates that administration of testosterone diminishes crying in young animals. This appears to be due to a change in the underlying sensitivity of the PANIC system. We have evaluated this possibility using ESB techniques in guinea pigs and have found that as animals get older, the sensitivity of the DV system diminishes; this effect is larger in males than in females.
...From this perspective, it is not surprising that crying and panic attacks are more common among women than among men.26 Such gender differences in emotionality may not simply be learned or culturally created phenomena.

One of the easiest ways to reduce the crying is to put mirrors on the wall of the test chamber. The chicks appear to behave as if they are in the company of others and cry less (see Figure 14.5).32 Similar reductions can be induced with music (see Figure 14.8), which may simulate the comfort derived from audiovocal contact with other animals. This may be one of the reasons people love music—it keeps them company.

Animals treated with moderate doses of opiates tend to socially isolate themselves. Rodents reduce the amount of time they spend in proximity to each other,40 dogs exhibit reduced tail wagging,41 primates exhibit decreased social grooming, and humans have also reported a decreased need to socialize.42 In other words, high opiate activity diminishes the underlying emotional need for companionship.

In general, though, when animals cannot experience opioid activity in the brain, they are more likely to socialize, if prevailing conditions are nonthreatening.

One easy way to study such effects objectively is to monitor crying in young animals that are held or not held. The effects are, of course, dramatic. Animals stop crying rapidly when gently touched. There is some evidence that this contact comfort is mediated, in part, by activation of brain opioid systems.

As we saw in the previous chapter, the most important work on the underlying nature of the social bond is emerging from empirical investigations based on two premises: the likelihood that the peripheral physiological processes that accompany birth may also control attachment processes in the brain, and that there are neurochemical similarities between opiate dependence and social dependence. Here I will amplify on these premises and also introduce a third, namely, that all neurochemistries that normally inhibit separation distress may also promote bonding.

In sum, the most reasonable supposition at present is that social bonding ultimately involves the ability of young organisms to experience separation distress when isolated from social support systems and to experience neurochemically mediated comfort when social contacts are reestablished.

Thus, separation distress may promote activity in fear circuits, but behavioral data suggest that the converse does not occur. For instance, the presentation of fearful stimuli tends to reduce the frequency of separation calls...

It is well documented that the major life factor in humans that precipitates depression is social loss.84 The genesis of many forms of depression can be linked to the neurobiological nature of the primal-loss experience—the despair of children who have been irreparably separated from their parents.

It is generally thought that there may be some evolutionary use for young organisms to exhibit a depressive response to separation after the initial protest response. After a period of intense vocalization, which could help parents find their lost offspring, it might be energetically adaptive to regress into a behaviorally inhibited despair phase in order to conserve bodily resources. Such a depressive state would help conserve limited energy resources and discourage the helpless organism from wandering even farther from safety. Silence would, of course, also minimize detection by predators. In other words, if initial protest did not achieve reunion, a silent despair response might still optimize the likelihood that parents would eventually find their lost offspring alive. No doubt the separation call returns in a periodic manner during the circadian cycle, but this issue remains unanalyzed.

Early childhood autism is characterized by severe failures in socialization, communication, and imagination. As Leo Kanner said in his seminal 1943 paper, autistic children “have come into the world with an innate inability to form the usual, biologically provided affective contact with people.”96 A current theoretical perspective is that these children do not develop a “theory of mind,” which refers to the ability of most children past the age of 2 to begin recognizing the types of thoughts and feelings that go on in the minds of others.97

 Chapter 15

Just as most young birds fly when the time is ripe, so do young mammals play when they have come of age.

Thus, the impulse for RAT [rough and tumble] play is created not from past experiences but from the spontaneous neural urges within the brain. Of course, a great deal of learning probably occurs during the course of roughhousing play, but this is ultimately the result of spontaneously active PLAY impulses within specific circuits of the brain, some of them in ancient parts of the thalamus, which coax young organisms to interact in ludic ways on the field of competition.

...[play] requires the right environment for full expression. For instance, fear and hunger can temporarily eliminate play.2 In most mammals, play emerges initially within the warm and supportive secure base of the home environment, where parental involvement is abundant.

The stronger urge for social dominance in males (which is only one component of RAT play) may have incorrectly led to the widespread supposition that roughhousing play impulses are more intense in males than in females. For instance, in humans, the apparent heightened male enthusiasm for rough sports may be due as much to their biologically and socially based “power needs” as to any intrinsic differences in the arousability of their basic PLAY circuits.

In most primates, prior social isolation has a devastating effect on the urge to play. After several days of isolation, young monkeys and chimps become despondent and are likely to exhibit relatively little play when reunited.6 Apparently, their basic needs for social warmth, support, and affiliation must be fulfilled first; only when confidence has been restored does carefree playfulness return.

Human play has been divided by social and developmental psychologists into exploratory/sensorimotor play, relational/functional play, constructive play, dramatic/symbolic play, and games-with-rules play, as well as RAT play, of course.

PLAY circuitry allows other emotional operating systems, especially social ones, to be exercised in the relative safety of one’s home environment. Play may help animals project their behavioral potentials joyously to the very perimeter of their knowledge and social realities, to a point where true emotional states begin to intervene. Thus, in the midst of play, an animal may gradually reach a point where true anger, fear, separation distress, or sexuality is aroused. When the animal encounters one of these emotional states, the playful mood may subside, as the organism begins to process its predicaments and options in more realistic and unidimensional emotional terms. In human children this may often consist of running to mother in tears, with complaints about the injustices they have encountered to see what type of social support and understanding (i.e., kin investment) they might be able to muster.
Finally, as will be discussed more fully later in this chapter, play and exploratory systems (i.e., of the type discussed in Chapter 8) appear to be distinct in the brain. Although these concepts are often combined in human research,16 as if they reflected synergistic processes, they appear to be independent and at times mutually exclusive. For instance, psychostimulants such as amphetamines, which invigorate exploratory activities, markedly reduce play behaviors.17 Indeed, when placed in new environments, animals typically exhibit strong exploratory activity with little tendency to play until they have familiarized themselves with the new surroundings.

Play dominance clearly emerges if two rats are allowed to play together repeatedly.20 After several play episodes, one rat typically tends to become the “winner,” in that it ends up on top more often during pins. On the average, the split is that the winner ends up on top about 70% of the time, while the “loser” achieves less success, but the continuation of play appears to require reciprocity and the stronger partner’s willingness to handicap itself. If one animal becomes a “bully” and aspires to end up on top all the time, playful activity gradually diminishes and the less successful animal begins to ignore the winner.

It is unlikely that professional football or other sports require the participation of PLAY circuits in adult humans, but the quality of performance is probably increased when such circuits are aroused. On the other hand, it is possible that few spectators would consider professional sports to be fun were it not for the existence of PLAY circuits in their brains that are vicariously aroused by observation of play activities in others.

Keeping “warrior energies” constrained within the guise of playfulness may help reduce the level of violence in peacetime. Indeed institutionalized forms of play, such as professional sports, have become big business around the world.

 Blind and Deaf Laughter

Apparently, laughter is not learned by imitation, since blind and deaf children laugh readily. The ability to laugh precedes one’s ability to comprehend the point of a joke; a great deal of children’s laughter typically occurs in free play situations rather than in response to verbal jests.

Laughter may now be one signal for victory within playful social encounters as the philosopher Thomas Hobbes argues,34 just as being in the top position during pinning in RAT play is the preferred physical position (Figures 15.2 and 15.3).

The apparent neural relationship between these two motor displays suggests that laughter and crying are intimately related in the brain, although the ability to cry appears to have preceded the ability to laugh in brain evolution.

The auditory system contributes positively to play to some extent, since deafened animals play slightly less, and rats do emit many 50-KHz laughter-type chirps both during play and in anticipation of play.39 However, the premier sensory system that helps instigate and sustain normal play is touch.

...[an] anesthetized animal still exhibits normal play-solicitation tendencies. The basic desire to play is not dependent on sensory inputs. It is an endogenous urge of the brain.

In other words, bilateral damage of the nonspecific reticular nuclei yields what appear to be specific play effects. Following such damage, pinning and dorsal contacts are both reduced, and the lesioned animals are no longer motivated to play. This effect is specific, since other relatively complex motivated behaviors, such as food seeking (foraging), are not diminished. This suggests that the parafascicular and posterior thalamic nuclei do specifically mediate play urges.

Likewise, a great number of environmental manipulations can reduce play—including all events that evoke negative emotional states such as fear, anger, and separation distress. In addition, hunger is a powerful inhibitor of play,53 as are many other bodily imbalances, including, of course, illness. In short, play is both a robust and a fragile phenomenon. When animals are healthy and feel good, play is an appealing psychobehavioral option. When they feel bad, it is not.

Activation of serotonergic and noradrenergic systems also reduces play, while receptor blockade of certain of these systems can increase play somewhat.60 Conversely, dopamine blockade reduces play, and most agonists do the same, which may indicate that animals need normal levels of synaptic dopamine activity in order to play.

The possible functions of play have been discussed extensively,63 and the proposed ideas are remarkably wide-ranging. Suggestions fall into two categories: social and nonsocial. Among the first are the learning of various competitive and noncompetitive social skills, ranging from behaviors that facilitate social bonding and social cooperation to those that promote social rank and leadership, as well as the ability to communicate effectively. Among the potential nonsocial functions are the ability of play to increase physical fitness, cognitive abilities, skillful tool use, and the ability to innovate. Innovation can range from very generalized cognitive skills such as the ability to think creatively in a wide range of situations to very specific aptitudes such as learning to hunt among young predators and predator-avoidance skills in prey species.

The best-documented beneficial effect of play discussed in the rodent behavioral literature is a mild increase in problem-solving ability in rats,66 but in unpublished work we have not been able to replicate this effect. Other reported effects are decreased habituation to novelty in animals that have not experienced normal amounts of juvenile play and increased fearfulness in social situations.67 Also, animals that have had much opportunity to play appear to be more effective in certain competitive encounters later in life,68 but more data must be collected on these issues.

One straightforward perspective is that during play all of the natural (unconditional) emotional-behavioral potentials of the brain can be exercised. However, in addition to the relatively obvious functional hypotheses summarized here, only a few of which have even modest empirical support, it is to be expected that play may also be important in the functional control of brain organization. ...A higher-level view is that play may serve to exercise and extend the range of behavioral options under the executive control of inborn emotional systems.72 In fact, play may be the waking functional counterpart of dreaming.

According to this view, play may serve a function that is orthogonal to that of REM sleep: Namely, REM may exercise the potentials for organizing affective information in emotional circuits, while play exercises the emotive behavioral potentials of these same circuits in the relative emotional safety of a positive affective state. In other words, dreaming and play may have synergistic functions—providing special opportunities for exercising the psychobehavioral potentials of emotional operating systems within socially supportive environments. Thus, there could be as many behavioral variants of play as there are primary emotional systems within the brain.

...one highly effective way to reduce RAT play in animals as well as in humans (as indicated by the observation of “hyperkinetic” children) is to administer psychostimulants such as amphetamines, which concurrently increase attention and investigatory activities. Such data raise the possibility that activities in PLAY and SEEKING systems may typically be antagonistic rather than synergistic.

At present, it seems reasonable to provisionally conclude that basic exploratory and PLAY circuits in the brain are distinct, and that they normally operate antagonistically. However, we should remain open to the possibility that vigorous activity of the SEEKING system is a source process for what is typically called object or manipulative play.

 Chapter 16

We humans can experience guilt, shame, embarrassment, jealousy, hate, and contempt, as well as pride and loyalty. However, in some yet undetermined manner, these secondary, cognitive-type emotions may also be linked critically to the more primitive affective substrates that we have discussed so far. Perhaps they emerge largely from social-labeling processes, whereby we experience slightly differing patterns of primitive feelings in various social contexts and come to accept them as distinct entities. Perhaps they reflect intermixtures of several basic emotions, even though no one has yet specified the proportions in the various recipes. However, they may also reflect newly evolved neural functions that have developed within the higher areas of the human brain. Perhaps human brain evolution yielded some totally new forms of affective-cognitive feelings, making us the complex creatures of history and culture that we are. No one really knows for sure, but it seems unlikely that those affective proclivities will ever be clarified at a neurological level, at least until the more primal passions are understood. I do not believe that distinct neurochemical systems will ever be found for such higher feelings, even though they may certainly have emerged from the evolutionary engraving of some additional paths of emotional epistemology within our general-purpose cerebral functions.

Affective neuroscience seeks to provide conceptual bridges that can link our understanding of basic neural circuits for the emotions with straightforward cognitive and folk-psychological views of the human mind and, most important, its emotional disorders. This interdisciplinary approach would have little chance of working were it not for the simple fact that we humans do have some introspective-linguistic access to our subjective feelings.6 Because of that small psychological window, and because the key emotional circuits are conserved in the brains of all mammals, the two can be linked in such a way that we can finally understand the neurobiological underpinnings of our human feelings. Conversely, and equally important, our introspective access to primitive feelings may also provide a credible scientific view, albeit indirect, on the minds of other animals.7 This conceptual bridge can yield clear empirical predictions in both directions, from animal to human and from human to animal, and it can serve as an intellectual highway for productive commerce between the psychosocial and neurobiological sciences, at least as far as the basic, genetically dictated foundations of our natures are concerned.

 Decorticate Competition

A similar conclusion is evident from the study of animals that have been decorticated early in life: They sustain a remarkably strong level of behavioral coherence and spontaneity. Indeed, as mentioned in the previous chapter, college students asked to observe two animals, one normal and one decorticate, typically mistake one for the other. This arises from the fact that decorticates are generally more active, while the normal animals appear more timid. Students tend to believe that the energized affective behavior is an indication of normality. The ability of such decorticate animals to compete effectively with normal animals during bouts of rough-and-tumble play is further testimony to the likelihood that internal self-coherence is subcortically organized.