Behave: The Biology of Humans at Our Best and Worst

by Robert M. Sapolsky

  Bare-Knuckled Female Aggression

  The traditional view is that other than maternal aggression, any female-female competition is passive, covert. As noted by the pioneering primatologist Sarah Blaffer Hrdy of the University of California at Davis, before the 1970s hardly anyone even researched competition among females.53

  Nevertheless, there is plenty of female-female aggression. This is often dismissed with a psychopathology argument—if, say, a female chimp is murderous, it’s because, well, she’s crazy. Or female aggression is viewed as endocrine “spillover.”54 Females synthesize small amounts of androgens in the adrenals and ovaries; in the spillover view, the process of synthesizing “real” female steroid hormones is somewhat sloppy, and some androgenic steroids are inadvertently produced; since evolution is lazy and hasn’t eliminated androgen receptors in female brains, there’s some androgen-driven aggression.

  These views are wrong for a number of reasons.

  Female brains don’t contain androgen receptors simply because they come from a similar blueprint as male brains. Instead, androgen receptors are distributed differently in the brains of females and males, with higher levels in some regions in females. There has been active selection for androgen effects in females.55

  Even more important, female aggression makes sense—females can increase their evolutionary fitness with strategic, instrumental aggression.56 Depending on the species, females compete aggressively for resources (e.g., food or nesting places), harass lower-ranking reproductive competitors into stress-induced infertility, or kill each other’s infants (as in chimps). And in the bird and (rare) primate species where males are actually paternal, females compete aggressively for such princes.

  Remarkably, there are even species—primates (bonobos, lemurs, marmosets, and tamarins), rock hyraxes, and rodents (the California mouse, Syrian golden hamsters, and naked mole rats)—where females are socially dominant and more aggressive (and often more muscular) than males.57 The most celebrated example of a sex-reversal system is the spotted hyena, shown by Laurence Frank of UC Berkeley and colleagues.* Among typical social carnivores (e.g., lions), females do most of the hunting, after which males show up and eat first. Among hyenas it’s the socially subordinate males who hunt; they are then booted off the kill by females so that the kids eat first. Get this: In many mammals erections are a sign of dominance, of a guy strutting his stuff. Among hyenas it’s reversed—when a female is about to terrorize a male, he gets an erection. (“Please don’t hurt me! Look, I’m just a nonthreatening male.”)*

  What explains female competitive aggression (in sex-reversal species or “normal” animals)? Those androgens in females are obvious suspects, and in some sex-reversal species females have androgen levels that equal or even trump those in males.58 Among hyenas, where this occurs, spending fetal life awash in Mom’s plentiful androgens produces a “pseudo-hermaphrodite”*—female hyenas have a fake scrotal sack, no external vagina, and a clitoris that is as large as a penis and gets erect as well.* Moreover, some of the sex differences in the brain seen in most mammals don’t occur in hyenas or naked mole rats, reflecting their fetal androgenization.

  This suggests that elevated female aggression in sex-reversal species arises from the elevated androgen exposure and, by extension, that the diminished aggression among females of other species comes from their low androgen levels.

  But complications emerge. For starters, there are species (e.g., Brazilian guinea pigs) where females have high androgen levels but aren’t particularly aggressive or dominant toward males. Conversely, there are sex-reversal bird species without elevated androgen levels in females. Moreover, as with males, individual levels of androgens in females, whether in conventional or sex-reversal species, do not predict individual levels of aggression. And most broadly, androgen levels don’t tend to rise around periods of female aggression.59

  This makes sense. Female aggression is mostly related to reproduction and infant survival—maternal aggression, obviously, but also female competition for mates, nesting places, and much-needed food during pregnancy or lactation. Androgens disrupt aspects of reproduction and maternal behavior in females. As emphasized by Hrdy, females must balance the proaggression advantages of androgens with their antireproductive disadvantages. Ideally, then, androgens in females should affect the “aggression” parts of the brain but not the “reproduction/maternalism” parts. Which is precisely what has evolved, as it turns out.*60

  Perimenstrual Aggression and Irritability

  Inevitably we turn to premenstrual syndrome (PMS)*—the symptoms of negative mood and irritability that come around the time of menstruation (along with the bloating of water retention, cramps, acne . . .). There’s a lot of baggage and misconceptions about PMS (along with PMDD—premenstrual dysphoric disorder, where symptoms are severe enough to impair normal functioning; it effects 2 to 5 percent of women).61

  The topic is mired in two controversies—what causes PMS/PMDD, and how is it relevant to aggression? The first is a doozy. Is PMS/PMDD a biological disease or a social construct?

  In the extreme “It’s just a social construct” school, PMS is entirely culture specific, meaning it occurs only in certain societies. Margaret Mead started this by asserting in 1928 in Coming of Age in Samoa that Samoan women don’t have mood or behavioral changes when menstruating. Since the Samoans were enshrined by Mead as the coolest, most peaceful and sexually free primates east of bonobos, this started trendy anthropological claims that women in other hip, minimal-clothing cultures had no PMS either.* And naturally, cultures with rampant PMS (e.g., American primates) were anti-Samoans, where symptoms arose from mistreatment and sexual repression of women. This view even had room for a socioeconomic critique, with howlers like “PMS [is] a mode for the expression of women’s anger resulting from her oppressed position in American capitalist society.”*62

  An offshoot of this view is the idea that in such repressive societies, it’s the most repressed women who have the worst PMS. Thus, depending on the paper, women with bad PMS must be anxious, depressed, neurotic, hypochondriacal, sexually repressed, toadies of religious repression, or more compliant with gender stereotypes and must respond to challenge by withdrawing, rather than by tackling things head on. In other words, not a single cool Samoan among them.

  Fortunately, this has mostly subsided. Numerous studies show normal shifts in the brain and behavior over the course of the reproductive cycle, with as many behavioral correlates of ovulation as of menses.*63 PMS, then, is simply a disruptively extreme version of those shifts. While PMS is real, symptoms vary by culture. For example, perimenstrual women in China report less negative affect than do Western women (raising the issue of whether they experience less and/or report less). Given the more than one hundred symptoms linked to PMS, it’s not surprising if different symptoms predominate in different populations.

  As strong evidence that perimenstrual mood and behavioral changes are biological, they occur in other primates.64 Both female baboons and female vervet monkeys become more aggressive and less social before their menses (without, to my knowledge, having issues with American capitalism). Interestingly, the baboon study showed increased aggressiveness only in dominant females; presumably, subordinate females simply couldn’t express increased aggressiveness.

  All these findings suggest that the mood and behavioral shifts are biologically based. What is a social construct is medicalizing and pathologizing these shifts as “symptoms,” a “syndrome,” or “disorder.”

  Thus, what is the underlying biology? A leading theory points to the plunging levels of progesterone as menses approaches and thus the loss of its anxiolytic and sedating effects. In this view, PMS arises from too extreme of a decline. However, there’s not much actual support for this idea.

  Another theory, backed by some evidence, concerns the hormone beta-endorphin, famed for being secreted during exercise and inducing a gauzy, euphoric “r
unner’s high.” In this model PMS is about abnormally low levels of beta-endorphin. There are plenty more theories but very little certainty.

  Now for the question of how much PMS is associated with aggression. In the 1960s, studies by Katharina Dalton, who coined the term “premenstrual syndrome” in 1953, reported that female criminals committed their crimes disproportionately during their perimenstrual period (which may tell less about committing a crime than about getting caught).65 Other studies of a boarding school showed a disproportionate share of “bad marks” for behavioral offenses going to perimenstrual students. However, the prison studies didn’t distinguish between violent and nonviolent crimes, and the school study didn’t distinguish between aggressive acts and infractions like tardiness. Collectively, there is little evidence that women tend toward aggression around their menses or that violent women are more likely to have committed their acts around their menses.

  Nevertheless, defense pleas of PMS-related “diminished responsibility” have been successful in courtrooms.66 A notable 1980 case concerned Sandie Craddock, who murdered a coworker and had a long rap sheet with more than thirty convictions for theft, arson, and assault. Incongruously but fortuitously, Craddock was a meticulous diarist, having years of records of not just when she was having her period but also when she was out about town on a criminal spree. Her criminal acts and times of menses matched so closely that she was put on probation plus progesterone treatment. And making the case stranger, Craddock’s doctor later reduced her progesterone dose; by her next period, she had been arrested for attempting to knife someone. Probation again, plus a wee bit more progesterone.

  These studies suggest that a small number of women do show perimenstrual behavior that qualifies as psychotic and should be mitigating in a courtroom.* Nevertheless, normal garden-variety perimenstrual shifts in mood and behavior are not particularly associated with increased aggression.

  STRESS AND IMPRUDENT BRAIN FUNCTION

  The time before some of our most important, consequential behaviors can be filled with stress. Which is too bad, since stress influences the decisions we make, rarely for the better.

  The Basic Dichotomy of the Acute and the Chronic Stress Response

  We begin with a long-forgotten term from ninth-grade biology. Remember “homeostasis”? It means having an ideal body temperature, heart rate, glucose level, and so on. A “stressor” is anything that disrupts homeostatic balance—say, being chased by a lion if you’re a zebra, or chasing after a zebra if you’re a hungry lion. The stress response is the array of neural and endocrine changes that occur in that zebra or lion, designed to get them through that crisis and reestablish homeostasis.*67

  Critical events in the brain mediate the start of the stress response. (Warning: the next two paragraphs are technical and not essential.) The sight of the lion activates the amygdala; amygdaloid neurons stimulate brain-stem neurons, which then inhibit the parasympathetic nervous system and mobilize the sympathetic nervous system, releasing epinephrine and norepinephrine throughout the body.

  The amygdala also mediates the other main branch of the stress response, activating the paraventricular nucleus (PVN) in the hypothalamus. And the PVN sends projections to the base of the hypothalamus, where it secretes corticotropin-releasing hormone (CRH); this triggers the pituitary to release adrenocorticotropic hormone (ACTH), which stimulates glucocorticoid secretion from the adrenals.

  Glucocorticoids plus the sympathetic nervous system enable an organism to survive a physical stressor by activating the classical “fight or flight” response. Whether you are that zebra or that lion, you’ll need energy for your muscles, and the stress response rapidly mobilizes energy into circulation from storage sites in your body. Furthermore, heart rate and blood pressure increase, delivering that circulating energy to exercising muscles faster. Moreover, during stress, long-term building projects—growth, tissue repair, and reproduction—are postponed until after the crisis; after all, if a lion is chasing you, you have better things to do with your energy than, say, thicken your uterine walls. Beta-endorphin is secreted, the immune system is stimulated, and blood clotting is enhanced, all useful following painful injury. Moreover, glucocorticoids reach the brain, rapidly enhancing aspects of cognition and sensory acuity.

  This is wonderfully adaptive for the zebra or lion; try sprinting without epinephrine and glucocorticoids, and you’ll soon be dead. Reflecting its importance, this basic stress response is ancient physiology, found in mammals, birds, fish, and reptiles.

  What is not ancient is how stress works in smart, socially sophisticated, recently evolved primates. For primates the definition of a stressor expands beyond merely a physical challenge to homeostasis. In addition, it includes thinking you’re going to be thrown out of homeostasis. An anticipatory stress response is adaptive if there really is a physical challenge coming. However, if you’re constantly but incorrectly convinced that you’re about to be thrown out of balance, you’re being an anxious, neurotic, paranoid, or hostile primate who is psychologically stressed. And the stress response did not evolve for dealing with this recent mammalian innovation.

  Mobilizing energy while sprinting for your life helps save you. Do the same thing chronically because of a stressful thirty-year mortgage, and you’re at risk for various metabolic problems, including adult-onset diabetes. Likewise with blood pressure: increase it to sprint across the savanna—good thing. Increase it because of chronic psychological stress, and you’ve got stress-induced hypertension. Chronically impair growth and tissue repair, and you’ll pay the price. Ditto for chronically inhibiting reproductive physiology; you’ll disrupt ovulatory cycles in women and cause plummeting erections and testosterone levels in men. Finally, while the acute stress response involves enhanced immunity, chronic stress suppresses immunity, increasing vulnerability to some infectious diseases.*

  We have a dichotomy—if you’re stressed like a normal mammal in an acute physical crisis, the stress response is lifesaving. But if instead you chronically activate the stress response for reasons of psychological stress, your health suffers. It is a rare human who sickens because they can’t activate the stress response when it is needed. Instead, we get sick from activating the stress response too often, too long, and for purely psychological reasons. Crucially, the beneficial effects of the stress response for sprinting zebras and lions play out over the course of seconds to minutes. But once you take stress to the time course of this chapter (henceforth referred to as “sustained” stress), you’ll be dealing with adverse consequences. Including some unwelcome effects on the behaviors that fill this book.

  A Brief Digression: Stress That We Love

  Either running from a lion or dealing with years of traffic jams is a drag. Which contrasts with stress that we love.68

  We love stress that is mild and transient and occurs in a benevolent context. The stressful menace of a roller-coaster ride is that it will make us queasy, not that it will decapitate us; it lasts for three minutes, not three days. We love that kind of stress, clamor for it, pay to experience it. What do we call that optimal amount of stress? Being engaged, engrossed, and challenged. Being stimulated. Playing. The core of psychological stress is loss of control and predictability. But in benevolent settings we happily relinquish control and predictability to be challenged by the unexpected—a dip in the roller-coaster tracks, a plot twist, a difficult line drive heading our way, an opponent’s unexpected chess move. Surprise me—this is fun.

  This brings up a key concept, namely the inverted U. The complete absence of stress is aversively boring. Moderate, transient stress is wonderful—various aspects of brain function are enhanced; glucocorticoid levels in that range enhance dopamine release; rats work at pressing levers in order to be infused with just the right amount of glucocorticoids. And as stress becomes more severe and prolonged, those good effects disappear (with, of course, dramatic individual differences as to where the transition from
stress as stimulatory to overstimulatory occurs; one person’s nightmare is another’s hobby).*

  Visit bit.ly/2ngw6bq for a larger version of this graph.

  We love the right amount of stress, would wither without it. But back now to sustained stress and the right side of the inverted U.

  Sustained Stress and the Neurobiology of Fear

  For starters, sustained stress makes people implicitly (i.e., not consciously) look more at angry faces. Moreover, during stress, that sensory shortcut from the thalamus to the amygdala becomes more active, with more excitable synapses; we know the resulting trade-off between speed and accuracy. Compounding things further, glucocorticoids decrease activation of the (cognitive) medial PFC during processing of emotional faces. Collectively, stress or glucocorticoid administration decreases accuracy when rapidly assessing emotions of faces.69

  Meanwhile, during stress things aren’t going great in the amygdala. The region is highly sensitive to glucocorticoids, with lots of glucocorticoid receptors; stress and glucocorticoids increase excitability of amygdaloid neurons,* particularly in the basolateral amygdala (the BLA), with its role in learning fear. Thus, this is another contingent hormone action—glucocorticoids don’t cause action potentials in amygdaloid neurons, don’t invent excitation. Instead they amplify preexisting excitation. Stress and glucocorticoids also increase levels of CRH in the BLA, and of a growth factor that builds new dendrites and synapses (brain-derived neurotrophic factor, or BDNF).70

  Recall from chapter 2 how during a fearful situation the amygdala recruits the hippocampus into remembering contextual information about the event (e.g., the amygdala remembers the thief’s knife, whereas the hippocampus remembers where the robbery occurred).71 Stress strengthens this recruitment, making the hippocampus a temporary fear-laden suburb of the amygdala. Thanks to these glucocorticoid actions in the amygdala,* stress makes it easier to learn a fear association and to consolidate it into a long-term memory.