International Congress on Universal Values and the Future of Society, São Paulo, September, 2001


We Are Not Prisoners of Our Brains

Daniel S. Levine, University of Texas at Arlington, Arlington, TX, USA

Riane Eisler, Center for Partnership Studies, Carmel, CA, USA

Sam Leven, For a New Social Science, Bethesda, MD, USA


Abstract: Considerable evidence exists both from laboratory animals and from humans that brain development is profoundly influenced after birth by social interactions. In humans this is most true before the age of about 7, but development of the frontal lobes, the major area involved in planning and in moral development, occurs through adolescence. Even in adult life, while new neural connections are seldom formed, existing neural connections are continually being strengthened or weakened by experience.

The complexity and plasticity of our brains argues against statements by sociobiologists that the possible forms of human societies are severely constrained by our genetics. We have capacities both for "fight-or-flight" responses and for what the social psychologist Shelley Taylor recently termed "tend-and-befriend" responses. This means that social and cultural organization both shapes and is shaped by our brain biochemistry. We will particularly review some early results by many research groups on the biochemistry of loving, caring, and positive social interactions, in which the hormone oxytocin (which seems to both release and be released by caring) plays a major role. Oxytocin interacts with neurotransmitters, such as dopamine, to reduce stress and to inhibit the negative effects of addictive drugs. Tentatively we suggest that this brain system for caring also inhibits the effects of other kinds of harmful addiction, such as addictions to violence, jealousy, unequal hierarchies, gender and racial stereotyping, and overwork.

Some sociobiological theories suggest that unequal economic and political hierarchies and sharp gender divisions are an inevitable result of our evolutionary adaptations as a species, and that the best we can do is try to be as cooperative as possible within these evolutionary constraints. Our work argues otherwise. It suggests that human nature is neither "good" nor "evil" but that genetics offers us a range of possible behavior patterns that social arrangements can either enhance or suppress. Organizing society to shift the balance in our brains toward caring is a matter of choice. We give a few examples in such areas as education, parenting, government policy, and social customs.


The Brain and the Future of Society

In a conference on values and the future of society, it is important to consider the human material that makes up society. What kinds of societies and institutions are we capable of? How do institutions affect the human beings in them? What beliefs about human nature and personality help us build a society that promotes the values we believe in? In this article we discuss some recent data from neuroscience and psychology that may bear on these questions.

Since beliefs have a great influence on behavior, changing society for the better involves more than "pragmatic" political and economic programs. It also involves adjusting our beliefs and attitudes. A growing number of people recognize that the early Twenty-first Century world is in a crisis largely of our own making, and that some shifts in our basic beliefs are necessary to survive this crisis. (1) The challenges of operating a global economy with world-wide communication links, and at the same time keeping alive a sense of community, minimizing violence, preserving our environment, and trying to eliminate poverty, make our beliefs more critical than ever.

Social change is inhibited by cynical attitudes about human possibilities for genuine cooperation, which dismisses the kind of solutions that genuinely work well as unrealistic. The sociologist C. Wright Mills (1958) called this kind of cynicism crackpot realism. One current example of crackpot realism relates to the environment. Continuation of "realistic" business practices regarding product use and waste management is likely to cause climate changes that will make our planet hard to live on. A special issue of Social Issues (Winter, 1995), devoted to the psychological changes necessary to support environmentally sound policies, concludes that we need to develop more optimistic beliefs about human nature.

Policy makers and business people infected with cynical beliefs about human nature are joined by many scientists, particularly those influenced by Sociobiology. The standard argument of sociobiologists is that essential parts of our makeup vary little if at all across cultures, since they arose as evolutionary adaptations (see, e.g., Pinker, 1997). Unequal social hierarchies of power and concentrations of wealth, so the argument goes, are due to evolution. Double standards for women and men, both in sexual and in interpersonal behavior, sociobiologists also say, arose out of the separate evolutionary adaptations of the "selfish genes" of males who have less investment in each offspring and females who have more investment. Attempts to transform society, they further claim, fly in the face of human nature -- so the best we can do is try to be as humane as possible within these cross-cultural genetic limitations on how caring we can be for each other and the planet.

We believe there are solid scientific arguments against this outlook. While unequal social hierarchies did indeed arise as evolutionary adaptations, so did cooperative partnerships. Reciprocity and social bonding are as fundamental to human evolution as are selfishness and domination. Humans as adults, even past reproductive age, must constantly make choices between alternative, and often conflicting, behavior patterns in their evolutionary repertoire.

Such choices would not be possible without the amazing plasticity of our brains. This means that not only our families but our societies, including both formal institutions and informal customs, have a great capacity to shape our brains and therefore our prevailing behaviors. In the last decade, increasing evidence has accumulated for long-lasting effects of childhood experience on the adult human brain.

Effects of Experience on the Brain

Babies do not have fully developed brains when they are born. If they did, they would not be able to fit through the birth canal. So the human brain must instead continue to develop outside the mother's womb for many years after the baby is born.

Psychologists have long told us that parents, other caregivers, and peers all have considerable influence on how a child develops. But we are also learning from neuroscience how deeply this influence affects brain structure and biochemistry.

The behavioral physiologist Donald Hebb (1949) proposed that such effects of experience could be mediated by a change at the synapse (connection) between two neurons (brain cells) if the two neurons are electrically active at about the same time. But most neurophysiologists resisted the idea of a change at the synapse until it was demonstrated by electrical recordings from single neurons. The first such demonstration was published in 1965 and occurred in California sea slug. The first such observation in a mammal was published in 1973 and occurred in the hippocampus, a memory encoding area, of the rabbit (Bliss & Lømo, 1973).

Because of such findings, most neuroscientists now agree that day-to-day events can cause changes in the chemistry of neural transmitters at some synapses. The exact biochemical mechanisms for these changes are not yet well worked out. Results are coming quickly, however, both from biochemical studies of neural transmitters and from imaging that indicates which regions of the brain are metabolically active in the presence of specific stimuli.

Such results suggest that if there is a pattern of stimulation, such as a pattern of caring or abusive treatment of a child, there would be lasting effects on synapses. And studies of chronically abused children confirm this supposition.

Humans and other animals possess an elaborate biological system for coping with stress. Responses in different parts of the brain, the endocrine glands, the immune system, and the cardiovascular system are coordinated to produce characteristic biochemical changes in response to unpleasant or potentially threatening environmental events. This interconnected system serves useful functions in evolution: it prepares the body for either fighting the stressful event or withdrawing from it.

Under normal circumstances, when the stressful events cease, the stress-based profile disappears and the body recovers its normal biochemical configuration. When the stresses are too severe or persistent, however, as with children who are physically or sexually abused repeatedly, the recovery cannot take place fast enough to keep up with the new stresses that occur. In this case, the biochemical configuration often changes permanently, with lasting damage to the personality.

The clinical neuroscientist Bruce Perry and his colleagues showed that responses to persistent trauma can take one of two general forms, or a combination of the two (Perry et al., 1995). One of these is the hyperarousal or fight-or-flight response. This is characterized by sensitization of pathways in the nervous system and other bodily organs (including the heart and endocrine glands) involved in responding to danger. This means the person becomes more likely to have an arousal response even to stimuli somewhat milder than the initial traumatic event.

The other form of response to trauma is the dissociative response. This is opposite to hyperarousal in that it involves freezing rather than fighting or fleeing. Dissociation is often accompanied by depression or a tendency to withdraw into fantasy or daydreaming, leading in some cases to addiction to alcohol or drugs.

The behaviors characteristic of the hyperarousal and dissociative responses involve changes in the available amounts of particular neural transmitters. These transmitters are the chemicals that control transmission of electrical signals at synapses between neuron. They work by binding chemically to a protein, called a receptor, at the cell that is receiving the signal.

A hyperarousal response to trauma involves an increase in activity of the brain's system for distribution of the transmitter norepinephrine (also known as noradrenalin). Norepinephrine is the transmitter most involved with fight and flight responses: with "pumping up" the brain's connections to the cardiovascular and endocrine systems involved in active responses to stressful situations. In children with typical hyperarousal patterns from early traumas, these receptors for norepinephrine have been shown to exhibit an altered pattern (Perry, 1988; Perry et al., 1995).

The long-term physiological changes in children exhibiting a dissociative pattern involve in some way the neural transmitter dopamine (Perry et al., 1995). This is the transmitter most involved with the rewarding effects of desirable stimuli (both natural positive reinforcers and addictive drugs), and with positive affect in general. Rather than mobilizing the organism toward a fighting or other coping response, it mobilizes the organism to withdraw emotionally from the current bad situation and try to "feel good." In contrast to the tendency of hyperaroused children toward a resting rapid heart rate, dissociated children tend toward hyperactivity of the vagus nerve which slows down the heart.

As Perry points out, the brain is malleable all through life, but much more so in the early years. Neural transmitter changes which influence learning in adult life actually impinge on neuron and nerve pathway growth in the young child. The result is that "states become traits" (Perry et al., 1995).

Perry reports that brain regions responsible for emotions, including attachment, are in the brains of severely abused children 20 to 30 percent smaller than in normal children. In adults who were abused as children the memory-making hippocampus is smaller than in nonabused adults. High levels of cortisol, a hormone involved in fight-or-flight, associated with trauma during the vulnerable early years also lead to deficits in attention regulation, self-control, and cognitive ability.

Hence, severe abuse and deprivation has lasting negative effects on the brain. But what about favorable early childhood experience? Does early pleasurable intellectual or emotional stimulation have a lasting positive effect on the adult brain?

Some animal studies show that an enriched environment has positive effects on the brain. An example is the studies by the neurophysiologist William Greenough and his colleagues of both sensory and motor areas of the brains of rats when placed in what they called an "enriched condition" environment (Jones et al., 1997; Kleim et al., 1998).

The enriched condition (EC) provided less stimulation than the natural environment of a wild animal but more than that of a typical laboratory rat: "EC rats were housed together for 60 days in a large wire mesh cage filled with a daily-changing set of toys and other objects. Once a day, animals were placed in an open field arranged with a new set of objects for 30 to 45 min." (Jones et al., 1997). The rats reared in enriched cages developed more of a certain type of synapse (called multiple synapses) on each neuron in the visual part of their cerebral cortex than did rats reared in standard laboratory cages. Scientists have suggested that these multiple synapses could be important for coherent responses to complex arrangements of stimuli.

Greenough and his colleagues found a similar enhancement of multiple synapses in the cerebellum, a part of the brain involved in motor control, when rats had been taught complex motor skills. They found that this synaptic enhancement was not simply an effect of motor activity but of motor skill learning. That is, rats who repeatedly ran a treadmill but did not acquire any new motor capability did not show such an enhancement.

These results, extrapolated to humans, suggest the importance of "learning by doing." And while this deals with motor skills, we can speculate that the same thing is true of interpersonal skills such as empathy.

In humans, the widely used noninvasive techniques for imaging the brain, such as positron emission tomography (PET) and magnetic resonance imaging (MRI), are not quite sensitive enough to yield results on the actual growth of connections. But even though the precise time course of brain growth in developing humans is still not completely known, we do know that the period from four to seven years of age is one of rapid growth of synapses. The neuropsychologists Jeri Janowsky and Ruth Carper (1996) describe the steps in brain development taking place in early school-age children as (1) neurons make connections to an appropriate target structure -- and make just the right number of synapses; (2) machinery is created for producing and releasing neurotransmitters; and (3) neurons become myelinated (surrounded by an insulating sheath of another type of cells called glial cells) to increase the efficiency of neural transmission.

Studies hint that both synaptic growth (processes # 1 and 2) and myelination (process #3) take place at different rates in different areas. In general, the more complex the functions of a brain region, the slower it reaches maturity. Those parts of the cerebral cortex that are called association cortex because they integrate and associate information from more than one sense (the major parts of the brain's parietal, temporal and frontal lobes) grow and myelinate slower than areas devoted to a single sense such as vision.

The frontal lobes, which are the main part of the brain for integrating instinct, emotion, and reason, for planning, and for moral development, do not seem to fully develop before puberty (Hudspeth & Pribram, 1990, 1992). Hudspeth and Pribram studied human brain development up to age 21 by analyzing frequencies in EEG (brain wave) patterns. They found that the pattern of EEG changes indicated the frontal lobes undergo a second growth spurt in late adolescence, approximately between the ages of 19 and 21. They interpreted these changes in brain wave patterns as representing maturation of neural structures in the frontal lobes during that age range.

The nature of the maturation might be myelination, that is, formation of the insulating "sheath" around brain cells that facilitates electrical transmission. Or it might be formation of new synapses. Either way, Hudspeth and Pribram's results on a key part of the human brain suggest that the life changes of late adolescence are likely to have formative influences on values and on prevalent behavior patterns into adulthood.

Heredity is Not Destiny

Separating exactly which aspects of human personality come from genes and which come from outside influences -- the family, schools, peer group, and societal customs -- is tricky. The studies summarized in the last section provide an ample basis for social and not just genetic influences on brain development. Yet there are social and economic forces propelling us to emphasize the genetic aspects of personality differences and to ignore those aspects generated by either the family or social institutions. One force, particularly in industrialized countries, is commercial.

When genetic aspects of personality and mental function are emphasized, people look to genetic engineering as a solution to some social problems. If we want to reduce crime, for example, this outlook says we should isolate "criminal genes" and try to reduce their prevalence in future generations. If we want to create future Einsteins, it says we should isolate genes that promote intellectual creativity and try to increase their prevalence in the next generation. If we want to increase the general level of medical care, it says we should look to high-tech modern medicine and genetic research as the main solution, ignoring other influences such as lifestyle and environment.

The social activist Jeremy Rifkin researched the growing biotechnology industry and its efforts to profit from patenting and marketing particular human genes. He noted that this industry depends on its scientific foundation: "A spate of new scientific studies on the genetic basis of human behavior and the new sociobiology that favors nature over nurture are providing a cultural context for the widespread acceptance of the new biotechnologies" (Rifkin, 1998, p. 12).

We believe that decisions about future generations of people are far too important to be handed over to a small group of individuals based on private profit. Besides, while some genetic treatments are likely to be of benefit in combating diseases with a known hereditary basis, including such mental diseases as schizophrenia, a focus on genetics alone harms society because it distracts us from thinking about important social influences on personality.

The need to identify violence-prone individuals, combined with the recent surge of interest in genetics, has spawned an interest in possible genetic determinants of caring behavior -- and of its extreme opposite, criminal behavior. Such studies as that of Raine et al. (2000) showing that men diagnosed with antisocial personality disorder have an average of 11 percent less gray matter in their frontal lobes than normal men, have been widely publicized.

Yet it is not clear from this study whether the lack of gray matter was primarily due to genes or environment. Moreover, another Raine study indicates that experience plays a role. This study focused on the relationship between traumas around the time of birth and violent crime in males around the age of 18 (Raine, Brennan, & Mednick, 1994). It showed that violent crimes were more likely to be committed by young men who had suffered both complications in the birth process and early maternal rejection. Maternal rejection was defined as an attempt to abort the fetus followed by placing the child in an institution in his first year. Neither maternal rejection nor birth complication alone predisposed the child to violence.

The Human Capacity for Caring and Uncaring Behaviors

What are the neural circuits and biochemical substances involved in either caring or uncaring behavior? And how is the release of these substances related to what we experience, both as children and adults?

We do not yet have systematic studies of effects of social environments on human brain biochemistry. But we know some of the neurochemical pieces involved. Other pieces we can intuitively gather from what we know of human emotional and behavioral responses.

Evidence from many sources, along with what we know in general about brain plasticity, suggests that positive experiences -- for adults as well as children -- should selectively strengthen neural circuits that represent positive emotions and caring social bonding. We have strong evidence about some of the biochemical substances involved. Two such substances are dopamine, one of our most important neurotransmitters, and oxytocin, one of our commonest peptide hormones.

Caring, Dopamine, and Oxytocin

Dopamine is the major transmitter involved in the brain's pleasure pathways, some of which come from dopamine producing neurons in the midbrain and go out both to the nucleus accumbens (one of the areas relating to emotion) and planning and working memory areas of the prefrontal cortex (furthest forward part of the frontal lobes) (Ashby, Isen & Turken, 1999; Schultz, Tremblay, & Hollerman, 2000). Figure 1 shows the location in the brain of these pathways and some others we mention.

 


Figure 1. Approximate location in the brain of some areas that are particularly important for affective regulation. Dark lines with arrows denote neural pathways connecting those areas. The top brain diagram highlights regions of the cerebral cortex (outer layer of the brain). The bottom brain diagram highlights subcortical regions which are largely common to humans and other mammals.

The dopamine inputs are believed to be important for the proper development of frontal lobe circuits in young children. This has been proposed as the mechanism by which proper caregiving, including pleasurable emotional experiences with parents or other caregivers, contributes essentially to the growth of a child's mental capacities.

Dopamine also probably plays a role in surges of both generosity and creativity in adults brought on by good moods. The social psychologist Alice Isen and her colleagues have done extensive experiments on people who are temporarily manipulated into having positive moods (e.g., Isen, 1999), by giving them candy or returning a coin after they made a paid telephone call. Isen's group found that mild positive moods cause people to stretch favorable categories of people further than they do in neutral moods, such as including bartenders as examples of nurturers. "Positive mood" subjects were also more generous than "neutral mood" subjects, contributing more to boxes set up in the room for charitable causes. Ashby et al. (1999) hypothesized that these positive moods involved release of dopamine to particular receptors.

Whereas dopamine is involved in a wide range of positive emotions, oxytocin is specifically involved in positive emotions relating to social and family connections. This hormone was first discovered to be essential for maternal behaviors such as uterine contraction and milk ejection. But Thomas Insel, James Winslow, and their colleagues discovered that oxytocin has broader importance for bonding, in male as well as female animals (e.g., Insel, 1992; Insel et al., 1998).

Insel and Winslow looked at two species of North American rodents that are closely related but have radically different social organization: the prairie vole, which is monogamous with strong male-female pair bonding and both parents involved in care of young, and the montane vole, which is promiscuous with fathers uninvolved with young. They found that oxytocin attaches to receptors in reward-related areas of the brain in the pair-bonding prairie vole but not in the non-bonding montane vole. Also, in female prairie voles, pair bonding -- with the first male they smell after reaching puberty -- can be induced by direct injections of oxytocin, and abolished by drugs that reduce the amount of oxytocin (Insel et al., 1998).

This pattern of oxytocin binding to reward sites in the brain seems to carry over to humans and apes, although this is less well established. There is also a variety of results suggesting that oxytocin inhibits both fight-or-flight and dissociative responses to stress, and instead promotes responding to stress by seeking positive social interactions and nonnoxious sensory stimulation. A subclass of these responses is what Taylor et al. (2000) termed tend-and-befriend. For simplicity, we take the liberty of using that term tend-and-befriend more broadly for all types of bonding or caring responses.

Uvnäs-Moberg (1997, 1998) reviews evidence from her laboratory and others that oxytocin administration in both male and female rats counteracts many typical physiological and behavioral effects of stress. For example, oxytocin causes decreases in blood pressure and in the amount of cortisol, a hormone typically released in stressful situations. More generally it reduces activity in the sympathetic part of the autonomic (i.e., "visceral") nervous system, which is the part activated in the fight-or-flight response.

The physiological antistress effects of oxytocin are known to occur in association with both lactation and sexual intercourse. What is less certain, but Uvnäs-Moberg also strongly suspects, is that oxytocin is also released by other forms of pleasurable social contact, such as mutual grooming in animals and supportive friendship in humans.

If oxytocin is indeed involved in a wide range of pleasurable experiences, this points to a physiological mechanism both for the health benefits of positive social experiences and for such therapies as massage. Turner et al. (1999) found that oxytocin levels in the blood of women who had never been pregnant increased in response to relaxation massage.

The evidence that oxytocin counteracts the dissociative response to stress comes particularly from the literature on addictive drugs. Drugs of abuse interact with the dopamine system, usually by increasing dopamine levels at the nucleus accumbens (see Figure 1), in a way that makes the maintenance of high dopamine levels dependent on the drug. But administration of oxytocin to rats and mice has been found to inhibit the development of drug tolerance, that is, the tendency to need progressively need larger doses, to several drugs including cocaine, morphine, heroin, and ethanol (Kovács, Sarnyai, & Szabó, 1998; Sarnyai & Kovács, 1994). The inhibition of tolerance also reduced symptoms from drug withdrawal. This seems to be mediated by interactions between oxytocin and a particular type of dopamine receptor.

We focus on oxytocin because of dramatic results linking that hormone both with positive social bonding (parental, sexual, or friendship-related) and with reduction of potentially unhealthy responses to stress. Yet there are also other substances important to the brain's caring system, such as two other peptide hormones, vasopressin and CCK; the class of peptides called beta endorphins; and the neurotransmitters dopamine and serotonin. Eisler, Levine, and Leven (2002) describe a few interactions among all these substances.

The Dynamics of Caring or Noncaring

All these results show that humans, like other mammals, have a genetic basis for caring behaviors. We also have a genetic basis for noncaring behaviors, which may be aggressive, defensive, or both, or else involve withdrawal from others.

However, we have much more complex brains than do rodents, due to our vastly expanded cerebral cortex. So while the fight-or-flight, dissociative, and tend-and-befriend systems are all still present in humans, how much each one is actually expressed, and how much this expression becomes part of each of our personality structure, depends heavily on how many positive or stressful life events we experience.

Through an elaborate network of brain connections, each of us has a different set of associations of other persons and objects with caring or noncaring. Some of the associations each of us has, our specific likes and dislikes, are probably inborn, but probably more of them are learned in the context of family and cultural upbringing.

But, particularly in humans, learning occurs at another level that is equally important. Persistent stress decreases the activity of the oxytocin system itself -- and therefore the ability to bond with anybody (Henry & Wang, 1998). Thus long-term negative experiences have lasting effects on brain chemistry which make future fight-or-flight or dissociative responses more likely and future tend-and-befriend responses less likely.

The long-term effects of positive experience on brain chemistry have been less studied. Yet such preliminary findings as those of Uvnäs-Moberg (1998) suggest that persistent positive social bonding or attachment experiences can increase levels of oxytocin and the parasympathetic nervous system pathways this hormone enhances, which tend to counterbalance activities of the sympathetic nervous system that promotes fight-or-flight.

This could help explain why societies, such as the Papago Indians of Arizona, in which parents tend to be lovingly attached to their children and not to use physical punishment, produce caring children (Eisenberg, 1992). It could also explain how the Klansman Larry Trapp converted to a much more caring and less prejudiced person after a positive encounter with a Jewish couple. It could explain why positive social bonds are the best predictor of health in elderly people.

It could explain how even mice genetically bred to be violent can become less violent in a supportive social setting. Gariépy et al. (1998) and Gariépy, Lewis, and Cairns (1996) bred mice to be either more and less aggressive and then reared them in isolation, which tends to reinforce aggressive tendencies, up to reaching puberty (about 45 days old). However, if the high-aggression mice were brought out of isolation and placed in groups between 45 and 69 days, many of them became less aggressive and more cooperative.

This experiment shows that genes do not solely determine behavior. It supports our hypothesis that what is most important is gene expression, that is, which of several possible genes is actually active in a given context. And it points to the importance of experience in gene expression.

The results of Gariépy's group argue strongly for the plasticity of brain systems mediating aggressive or cooperative behavior. Just bringing the mice into social groups, without deliberately structuring the groups cooperatively, made them more cooperative than their prevalent genes would lead us to expect. Extrapolating from mice to humans is difficult because human social interactions are more complex. Yet the finding on behavioral plasticity in mice suggests at least as much plasticity in humans. This supports the belief that while people may differ genetically in their capacities for caring or altruistic behavior, even those at the low end of the capacity scale can engage in caring behavior if their social contexts are structured in a way to encourage such behavior.

The neural dynamics mediating such selective gene expression are not yet known. But we know some of the neural pathways for all three types of responses we mention -- fight-or-flight (hyperarousal), dissociative, and tend-and-befriend. These pathways are described in detail elsewhere (Eisler et al., 2002) and we now summarize them briefly with the aim of discussing how the brain (particularly, the prefrontal cortex) regulates which of these response classes is most active at a given time.

Brain Pathways for Hyperarousal and Dissociation

If stresses are too persistent, or if past stresses or absence of positive social contact have suppressed the oxytocin-based bonding system, the brain's hyperarousal or dissociative systems in become chronically active. One of the deciding factors as to which of those two systems is activated is whether the person feels that she or he is helpless in the situation. People who feel able to escape or fight against a threat tend to do so, whereas those who feel helpless tend to dissociate (Henry & Wang, 1998).

Both fight-or-flight and dissociative responses involve activity of pathways connecting the hypothalamus (see Figure 1) with two important endocrine glands, the pituitary and adrenal glands. These pathways, known as the hypothalamic-pituitary-adrenocortical (HPA) axis, are involved in production of the hormone cortisol which is typically released during stress. These systems are active in normal individuals during acute stress situations and changes in receptor properties make them chronically active in individuals who have been abused or otherwise undergone trauma.

As we saw earlier, another substance typically released during fight-or-flight responses is the neurotransmitter norepinephrine. There are extensive interactions in the brain between these two "fight-or-flight" substances, cortisol and norepinephrine (Koob, 1999). These involve positive feedback loops including parts of the amygdala (see Figure 1), which process the degree of fearfulness associated with stimuli in the environment; parts of the hypothalamus, which regulate endocrine secretion; and a brainstem area called the locus coeruleus which is the source of most of the norepinephrine synapses going to other parts of the brain.

All those brain areas in turn generate behavioral responses to stress (fighting or fleeing) as well as responses of both the HPA axis (endocrine) and the sympathetic nervous system (which affects the viscera). This self-perpetuating biochemical activity tends to enhance and perpetuate the hyperarousal response once it gets going, unless the external environment becomes much less stressful.

We expect chronic stress -- such as childhood abuse -- to make this system more excitable so that even mildly unpleasant events can generate activity in this positive feedback loop. This potentiates the fight-or-flight response so that the person or animal responds to even minor discomfort with massive production of both cortisol and norepinephrine. This in turn leads to typical sympathetic nervous system responses such as increases in heart rate, blood pressure, and metabolic rate.

In dissociative responses, based on work summarized by Perry et al. (1995) and Henry and Wang (1998), we expect some of the same brain areas to be involved as in fight-or-flight responses, but with less norepinephrine activity in dissociated individuals. Dissociation is like fight-or-flight in that cortisol levels are generally high and oxytocin levels low.

Dissociative responses involve dysfunctions of the reward system in which dopamine is the most important neurotransmitter. Dissociation typically means that enduring rewards of positive social interactions are less available. Consequently, dissociated people tend to continually seek rewards from objects, or from mental states such as fantasy, that provide only short-term satisfaction.

Since drug addiction is a form of dissociation, we can turn to the literature on neurobiology of addiction for clues as to more general dissociative responses. Koob and LeMoal (2001) noted that drugs of abuse tend to interact with the brain's reward system in such a way that once a drug has become associated with reward, progressively more of the drug is needed to achieve the same state of reward. They reviewed evidence that excess cortisol disrupts the proper functioning of the brain's reward system by generating compulsive activity in a circuit that includes the prefrontal cortex and parts of the thalamus and basal ganglia (see Figure 1). As a result of this compulsive neural activity, behavior that once led to pleasure is compulsively repeated even after it leads to much less pleasure.

Brain Pathways for Caring

Since a version of the tend-and-befriend (bonding) response is found in voles, we start with a theory of bonding based on how, in the simpler brains of these animals, the peptide hormone oxytocin mediates differences in bonding patterns between prairie and montane voles (Insel et al., 1998), along with another hormone called vasopressin that is particularly important to pair bonding in male voles.

Our theory of bonding is based on differences between the brains of the two vole species with different bonding patterns. Our assumption is that if we identify those brain regions that oxytocin and vasopressin bind more to in the pair-bonding prairie vole than in the non-bonding montane vole, we will have identified regions that in both voles and humans play a role in bonding behavior.

Insel et al. (1998) review data suggesting that the key area for oxytocin binding seems to be the nucleus accumbens (see Figure 1), part of the dopamine-modulated stimulus-response system. The key area for vasopressin bonding seems to be an area called the diagonal band that produces the neurotransmitter acetylcholine, which is believed to be involved in selective attention (Everitt & Robbins, 1997). These data suggest complementary roles for the two hormones in bonding, with oxytocin more related to the part of the process that drives behavior via reward, and vasopressin more related to the part of the process that focuses attention on the individual with which the particular vole is forming a pair bond.

In voles, the tendency to seek social and sexual stimulation becomes conditioned to a particular partner of the opposite sex (the one first encountered after puberty). As evolution proceeds from voles to humans, conditioning becomes far more complex. For example, humans undergo conditioning not just about whom to bond with, but about how strong is the tendency to bond with anybody, as opposed to engaging in fight-or-flight or dissociative behavior. Moreover, humans are affected by social and cultural conditioning (e.g., cultural pressures to bond with some groups of people and not bond with others).

In the process of the brain's evolution from reptiles to non-primate mammals to humans and other primates, most structural and functional systems found in the earlier species are preserved as additional mental capacities develop due to massive growth of the cerebral cortex. Specifically, the subcortical system of socially based affective regulation shared with rodents now interacts, by extensive feedback connections, with networks in the cortex that process complex social stimuli, rewards, rules, and customs not found in rodents.

In humans, the key cortical area for affective regulation is likely to be the orbital and medial part of the prefrontal cortex, the primary cortical terminus of the limbic system (Figure 1) which relates to emotion (Damasio, 1994).

The Role of the Orbitomedial Prefrontal Cortex

The orbital and medial prefrontal cortex has long been recognized as the part of the human brain that uniquely mediates complex emotional responses including social responses. The famous 19th century patient Phineas Gage lost the ability to make plans and respond appropriately to situations after an accident in which an iron rod went through his head, and a mechanical reconstruction by the contemporary neuroscientist Antonio Damasio and his colleagues (Damasio, 1994) showed that the orbitomedial prefrontal cortex was where Gage had been most damaged. This region is unique in the extent of its connections both to sensory and association areas of the cortex and to the areas described in the last few sections (hypothalamus, amygdala, and basal ganglia; see Figure 1) with extensive visceral projections.

Neuroscientists have reached a consensus, from varied clinical and lesion studies, that the orbitomedial prefrontal cortex forms and sustains mental linkages between specific sensory events in the environment -- for example, particular people or family or social structures -- and particular positive or negative emotional states. It is widely believed that the prefrontal cortex sustains connections between neural activity patterns in the cortex that reflect the influence of past sensory events, and other neural activity patterns in autonomic regions that reflect innate or learned expressions of emotional states

It seems a plausible speculation that the area of the brain mediating the emotional significance a person attaches to events also mediates the prevalence of large classes of responses such as fight-or-flight, dissociation, and tend-and-befriend. How might this occur?

The orbitomedial prefrontal cortex is likely to operate via reciprocal connections with several of the subcortical brain areas involved in both caring and uncaring responses. One of them is a part of the hypothalamus called the paraventricular nucleus (PVN) which is involved in regulating endocrine secretion (Buijs & Van Eden, 2000). Different parts of the PVN contain, among other hormones, oxytocin, vasopressin, and the precursor of the stress hormone cortisol. The prefrontal cortex can selectively enhance the activity of one of these parts of PVN, through its synapses on other parts of the hypothalamus that in turn connect to PVN..

This use of inhibition allows the orbitomedial prefrontal cortex to play a role in selection between competing responses to both external stimuli and internal states. This area of cortex has evolved in humans to enable us to make these behavioral choices in an increasingly complex social environment (Damasio, 1994). The types of behavior that prefrontal regulation tends to release (by inhibiting competing behaviors) are likely to be those that are encouraged by the society and family that a person interacts with.

Specifically, we hypothesize that for a person in a supportive environment, or making a conscious choice to engage in more caring behavior, the orbitomedial prefrontal cortex is involved in releasing her or his caring capacities, by preventing their inhibition by emotionally stressful stimuli and beliefs.

Based on this simplified schema, we can conjecture that at any given time the prefrontal cortex sends different strengths of signals to the different parts of PVN that contain oxytocin or the cortisol precursor, and that this can be a means of influencing the relative likelihood of oxytocin-mediated (tend-and-befriend) versus cortisol-mediated (fight-or-flight or dissociative) responses. Since the orbitomedial prefrontal cortex seems to store the emotional or visceral significance of social memories, the relative strengths of these pathways could be influenced by the amount of stress in the early years.

Whatever the brain locus at which such conditioning operates, the prefrontal cortex's selection of behavior can be biased in the direction of whatever sets of behaviors are favored by parents and/or society at large, including influences from education, media, politics, economics, and religion.

How Does Society Interact With Our Brains?

Eisler (1987, 1995) argues that throughout history there has been a conflict between those who would inhibit uncaring behavior in order to promote mutually respectful and caring relations, and those who would inhibit caring behavior in order to protect social hierarchies. Beliefs, institutions, and behaviors required to maintain hierarchies of control are often seen as normal, including massive economic inequalities, rigid sex role divisions, and environmentally unsound business practices.

In our neuroscience framework, such behaviors are viewed not as normal but rather as the results of interactions among large numbers of people whose brains have been disrupted by the chronic stresses inherent in establishing and maintaining hierarchies of domination backed up by fear and force. This is a type of hierarchy that is very different from a hierarchy of actualization, as in the contemporary movement to redefine the manager from cop and controller to facilitator and mentor.

Drug addiction provides a model for understanding these dynamics. Recall from the last section that drug addiction often leads to repetitive activity in a loop including several brain areas, which in turn drives the compulsion to engage in certain behaviors even after they no longer lead to pleasure. We conjecture that similar dynamics may be occurring for many other "addictive" noncaring behavior patterns, including domestic violence and other criminal behaviors, working long hours to the neglect of family life, and running corporations without regard for human welfare.

So when we engage in uncaring behavior, we may be trapped in a compulsive pattern, or not know we have an alternative. This means the availability of an alternative can lead to a readjustment, regulated by the prefrontal cortex, of the set points for reward that the uncaring behavior disrupted. This suggests that uncaring behavior is reversible when there is sufficient social support.

Historical examples abound of people overcoming whatever genetic tendencies they have to be uncaring. Entrenched traditions of domination, such as the "divinely ordained" right of kings to rule and of men to control the women and children in their homes, have been challenged over the last 300 years. The 19th century Social Darwinist beliefs in the intellectual superiority of white to darker-skinned races and of men to women have been proved false. Nations such as Norway, Sweden, and Finland have in the last century developed societies with no huge gaps between haves and have-nots, women being approximately 35-40 percent of the elected officials, and social policies that encourage caring for children, the elderly, and the environment. Finally, archeological data indicate that many prehistoric societies oriented more than current ones toward the partnership model -- societies where we find art idealizing not conquest and domination but the nurturing powers of nature and of woman's body (Eisler, 1987, 1995).

The Bottom Line: Neuroscience Supports Progressive Social Values

Our goal is applying what knowledge we have to increasing the level of caring and cooperation in the world. With this goal in mind, what are some take-home messages of the studies we report from neuroscience, experimental psychology, and clinical neuropsychology?

The first take-home message is that the question of "nature versus nurture" is not the most productive question to ask. The nature-nurture distinction is an artefact, because brain pathways continue to be laid down after birth, and those pathways most responsible for our unique personalities continue to be laid down through puberty. Even later, what behavioral possibilities are expressed largely hinges on family, educational, work, and other social, economic, and cultural cues.

A more fruitful question to ask is "what forms of nurture bring out the most desirable qualities in human nature?" We use "nurture" more broadly than just primary caregiving and the home environment, though those are extremely important. We also include influences on the child's development from schools, religious institutions, the mass media, and social programs such as day care and youth recreation facilities. And we use "human nature" to describe a genetically derived range of possible neural responses and behaviors.

The second message is that caring or noncaring people are not born so much as they are made by circumstances and their own choices. At least some violent people are changeable by outside influences. A real-life recent example in the United States was Larry Trapp, an officer in Nebraska of the racist Ku Klux Klan, who changed from an advocate of hate, prejudice, and violence to an advocate of racial and religious tolerance and caring. This dramatic change was brought about by his relationship with a courageous Jewish couple who had responded with caring to his hate messages (Dallas Morning News, September 9, 1992).

While some criminals may be deficient in brain pathways involved in empathy, this may not be the majority of criminals. And even those who do have brain damage often have acquired it through childhood abuse or head injury. It is even less likely that brain damage accounts for the behavior of people who are part of a destructive system, such as Nazi officials or executives of polluting corporations.

Most of us have a genetic spectrum that can range between acts of the most heroic empathic caring and acts of the most unfeeling cruelty. Cruelty is related to excessive activity of a "fight-or-flight" system in the brain designed to cope with threats to survival. Caring is related to the activity of a system in the brain designed to promote cooperation, love, and family and social bonding. Both of these systems are necessary for our effective functioning, and both are the products of millions of years of evolution across reptiles and mammals. Maintaining the balance between the fight-or-flight and bonding systems is delicate. The results we cite indicate that the amount of stress in the social environment has a great effect on the balance point between these two systems.

The final, and most important, message is that science supports the belief that both social policies and social customs make a difference in human behavior. The enormous effects of positive or negative childhood experience on the adult brain supports the conclusion that a basic investment by society in quality child care, education, and family-friendly employment and vacation policies is not only morally right but economically sound. This means that the "race to the bottom" of social welfare and wages occurring in the early stages of economic globalization needs to be replaced by a world-wide adoption of policies similar to those that have been adopted in the last half century in much of western Europe. Details of such policies are omitted for space reasons, but many can be found in Eisler (1995, 2000), and on the web site www.partnershipway.org in the interviews with Riane Eisler entitled Building a Just and Caring World, Economics Keynote Lecture, and Reclaiming our Humanity.

These same books and interviews also give examples of changes that need to take place at the level of customs. These involve reclaiming the emphasis of partnership as opposed to domination as the cornerstone of human relations. This means that many uncaring relationships which have been accepted as normal need to be seen instead as aberrations that society should strongly discourage. One example is school bullying, which has received much attention since the 1999 mass shooting at Columbine High School in Colorado (Aronson, 2000). Others include male oppression of women, eroticization of violence, repression of sexual pleasure, overpopulation due to restrictions on contraception, religious glorification of self-induced pain, and cultural glorification of war.

These can be replaced by a valuing of pleasure-based partnership and reciprocity, a positive, spiritual view of sexuality, and cultural glorification of peace. Our brains do not guarantee that we will do so, but provide the capacities for doing so..

References

Aronson, E. (2000). Nobody Left to Hate. New York: Worth.

Bliss, T., & Lømo, T. (1973). Journal of Physiology (London), 232, 331-356.

Buijs, R., & Van Eden, C. (2000). Progress in Brain Research, 127, 117-132.

Damasio, A. (1994). Descartes' Error. New York: Grosset/Putnam.

Eisenberg, N. (1992). The Caring Child. Cambridge, MA: Harvard University Press.

Eisler, R. (1987). The Chalice and the Blade. San Francisco: Harper.

Eisler, R. (1995). Sacred Pleasure. San Francisco: Harper.

Eisler, R. (2000). Tomorrow's Children. Boulder, CO: Westview.

Eisler, R., Levine, D., & Leven, S. (2002). Brain and Mind, to appear.

Everitt, B., & Robbins, T. (1997). Annual Review of Psychology, 48, 649-684.

Gariépy, J.-L., Gendreau, P., Cairns, R., & Lewis, M. (1998). Behavioural Brain Research, 95, 103-111.

Gariépy, J.-L., Lewis, M., & Cairns, R. (1996). In D. Stoff, R. Cairns et al. (Eds.). Aggression and Violence: Genetic, Neurobiological, and Biosocial Perspectives. Mahwah, NJ: Erlbaum.

Hebb, D. (1949). The Organization of Behavior. New York: Wiley.

Henry, J., & Wang, S. (1998). Psychoneuroendocrinology, 23, 863-875.

Hudspeth, W., & Pribram, K. (1990). Journal of Educational Psychology, 82, 881-884.

Hudspeth, W., & Pribram, K. (1992). International Journal of Psychophysiology, 12, 19-29.

Insel, T. (1992). Psychoneuroendocrinology 1992, 17, 3-33.

Insel, T., Winslow, J., Wang, Z., & Young, L. (1998). In H. Zingg, C. Bourque, & D. Bichet (Eds.), Vasopressin and Oxytocin: Molecular, Cellular, and Clinical Advances (pp. 215-230). New York: Plenum.

Isen, A. (1999). In T. Dalgleish, M. Power et al (Eds.), Handbook of Cognition and Emotion (pp. 521-539). Chichester, England: Wiley.

Janowsky, J., & Carper, R. (1996). In A. Sameroff & M. Haith (Eds.), The Five to Seven Year Shift: The Age of Reason and Responsibility (pp. 33-60). Chicago: University of Chicago Press.

Jones, T., Klintsova, A., Kilman, V., Sirevaag, A., & Greenough, W. (1997). Neurobiology of Learning and Memory,68, 13-20.

Kleim, J., Pipitone, M., Czerlanis, C., & Greenough, W. (1998). Neurobiology of Learning and Memory, 69, 290-306.

Koob, G. (1989). Biological Psychiatry, 46, 1167-1180.

Koob, G., & LeMoal, M. (2001). Neuropsychopharmacology, 24, 97-129.

Kovács, G., Sarnyai, Z., & Szabó, G. (1998). Psychoneuroendocrinology, 23, 945-962.

Mills, C. W. (1958). The Causes of World War Three. New York: Simon and Schuster.

Perry, B. (1988). Progress in Brain Research, 73, 189-205.

Perry, B., Pollard, R., Blakley, T., Baker, W., & Vigilante, D. (1995). Infant Mental Health Journal, 16, 271-291.

Pinker, S. (1997). How the Mind Works. Cambridge, MA: MIT Press.

Raine, A., Brennan, P., & Mednick, S. (1994). Archives of General Psychiatry, 51, 982-988.

Raine, A., Lencz, T., Bihrle, S., LaCasse, L., & Colletti, P. (2000). Archives of General Psychiatry, 57, 119-127.

Rifkin, J. (1998). The Nation, April 13, 1998, 11-19.

Sarnyai, Z., & Kovács, G. (1994). Psychoneuroendocrinology, 19, 85-117.

Schultz, W., Tremblay, L., & Hollerman, J. (2000). Cerebral Cortex, 10, 272-283.

Taylor, S., Klein, L., Lewis, B., Gruenewald, T., Gurung, R,. & Updegraff, J. (2000). Psychological Review, 107, 411-429.

Turner, R., Altemus, M., Enos, T., Cooper, B., & McGuinness, T. (1999). Psychiatry, 62, 97-113.

Uvnäs-Moberg, K. (1997). Acta Physiologica Scandinavica, 640 (Suppl.), 38-42.

Uvnäs-Moberg, K. (1998). Psychoneuroendocrinology, 23, 819-835.

1. A summary of statements about the crisis and opportunity of the new millennium by over sixty religious, political, scientific, and literary leaders, appears in the January/February 2000 issue of Tikkun..