Behave: The Biology of Humans at Our Best and Worst PDF

 ALSO BY ROBERT M. SAPOLSKY Monkeyluv and Other Essays on Our Lives as Animals A Primate’s Memoir The Trouble with Testosterone and Other Essays on the Biology of the Human Predicament Why Zebras Don’t G...

 ALSO BY ROBERT M. SAPOLSKY Monkeyluv and Other Essays on Our Lives as Animals A Primate’s Memoir The Trouble with Testosterone and Other Essays on the Biology of the Human Predicament Why Zebras Don’t Get Ulcers: A Guide to Stress, Stress-Related Diseases, and Coping Stress, the Aging Brain, and the Mechanisms of Neuron Death  PENGUIN PRESS An imprint of Penguin Random House LLC 375 Hudson Street New York, New York 10014 penguin.com Copyright © 2017 by Robert M. Sapolsky Penguin supports copyright. Copyright fuels creativity, encourages diverse voices, promotes free speech, and creates a vibrant culture. Thank you for buying an authorized edition of this book and for complying with copyright laws by not reproducing, scanning, or distributing any part of it in any form without permission. You are supporting writers and allowing Penguin to continue to publish books for every reader. Illustration credits appear here. Library of Congress Cataloging-in-Publication Data Names: Sapolsky, Robert M., author. Title: Behave: the biology of humans at our best and worst / Robert M. Sapolsky. Description: New York: Penguin Press, 2017. Identifiers: LCCN 2016056755 (print) | LCCN 2017006806 (ebook) | ISBN 9781594205071 (hardback) | ISBN 9780735222786 (ebook) Subjects: LCSH: Neurophysiology. | Neurobiology. | Animal behavior. | BISAC: SCIENCE / Life Sciences / Biology / General. | SOCIAL SCIENCE / Criminology. | SCIENCE / Life Sciences / Neuroscience. Classification: LCC QP351.S27 2017 (print) | LCC QP351 (ebook) | DDC 612.8–dc23 LC record available at https://lccn.loc.gov/2016056755 Interior Illustrations by Tanya Maiboroda here, here, here, here, here, here, here, here, here, here, here, here, here, here, here, here, here, here, here, here, here, here, here, here, here, here Version_1  To Mel Konner, who taught me. To John Newton, who inspired me. To Lisa, who saved me.  Contents Also by Robert M. Sapolsky Title Page Copyright Dedication INTRODUCTION One THE BEHAVIOR Two ONE SECOND BEFORE Three SECONDS TO MINUTES BEFORE Four HOURS TO DAYS BEFORE Five DAYS TO MONTHS BEFORE Six ADOLESCENCE; OR, DUDE, WHERE’S MY FRONTAL CORTEX? Seven BACK TO THE CRIB, BACK TO THE WOMB Eight BACK TO WHEN YOU WERE JUST A FERTILIZED EGG Nine CENTURIES TO MILLENNIA BEFORE Ten THE EVOLUTION OF BEHAVIOR Eleven US VERSUS THEM Twelve HIERARCHY, OBEDIENCE, AND RESISTANCE Thirteen MORALITY AND DOING THE RIGHT THING, ONCE YOU’VE FIGURED OUT WHAT THAT IS Fourteen FEELING SOMEONE’S PAIN, UNDERSTANDING SOMEONE’S PAIN, ALLEVIATING SOMEONE’S PAIN Fifteen METAPHORS WE KILL BY Sixteen BIOLOGY, THE CRIMINAL JUSTICE SYSTEM, AND (OH, WHY NOT?) FREE WILL Seventeen WAR AND PEACE EPILOGUE Acknowledgments Appendix 1: Neuroscience 101 Appendix 2: The Basics of Endocrinology Appendix 3: Protein Basics Glossary of Abbreviations Notes Illustration Credits Index About the Author  Introduction T he fantasy always runs like this: A team of us has fought our way into his secret bunker. Okay, it’s a fantasy, let’s go whole hog. I’ve single- handedly neutralized his elite guard and have burst into his bunker, my Browning machine gun at the ready. He lunges for his Luger; I knock it out of his hand. He lunges for the cyanide pill he keeps to commit suicide rather than be captured. I knock that out of his hand as well. He snarls in rage, attacks with otherworldly strength. We grapple; I manage to gain the upper hand and pin him down and handcuff him. “Adolf Hitler,” I announce, “I arrest you for crimes against humanity.” And this is where the medal-of-honor version of the fantasy ends and the imagery darkens. What would I do with Hitler? The viscera become so raw that I switch to passive voice in my mind, to get some distance. What should be done with Hitler? It’s easy to imagine, once I allow myself. Sever his spine at the neck, leave him paralyzed but with sensation. Take out his eyes with a blunt instrument. Puncture his eardrums, rip out his tongue. Keep him alive, tube-fed, on a respirator. Immobile, unable to speak, to see, to hear, only able to feel. Then inject him with something that will give him a cancer that festers and pustulates in every corner of his body, that will grow and grow until every one of his cells shrieks with agony, till every moment feels like an infinity spent in the fires of hell. That’s what should be done with Hitler. That’s what I would want done to Hitler. That’s what I would do to Hitler. — I’ve had versions of this fantasy since I was a kid. Still do at times. And when I really immerse myself in it, my heart rate quickens, I flush, my fists clench. All those plans for Hitler, the most evil person in history, the soul most deserving of punishment.  But there is a big problem. I don’t believe in souls or evil, think that the word “wicked” is most pertinent to a musical, and doubt that punishment should be relevant to criminal justice. But there’s a problem with that, in turn—I sure feel like some people should be put to death, yet I oppose the death penalty. I’ve enjoyed plenty of violent, schlocky movies, despite being in favor of strict gun control. And I sure had fun when, at some kid’s birthday party and against various unformed principles in my mind, I played laser tag, shooting at strangers from hiding places (fun, that is, until some pimply kid zapped me, like, a million times and then snickered at me, which made me feel insecure and unmanly). Yet at the same time, I know most of the lyrics to “Down by the Riverside” (“ain’t gonna study war no more”) plus when you’re supposed to clap your hands. In other words, I have a confused array of feelings and thoughts about violence, aggression, and competition. Just like most humans. To preach from an obvious soapbox, our species has problems with violence. We have the means to create thousands of mushroom clouds; shower heads and subway ventilation systems have carried poison gas, letters have carried anthrax, passenger planes have become weapons; mass rapes can constitute a military strategy; bombs go off in markets, schoolchildren with guns massacre other children; there are neighborhoods where everyone from pizza delivery guys to firefighters fears for their safety. And there are the subtler versions of violence— say, a childhood of growing up abused, or the effects on a minority people when the symbols of the majority shout domination and menace. We are always shadowed by the threat of other humans harming us. If that were solely the way things are, violence would be an easy problem to approach intellectually. AIDS—unambiguously bad news—eradicate. Alzheimer’s disease—same thing. Schizophrenia, cancer, malnutrition, flesh- eating bacteria, global warming, comets hitting earth—ditto. The problem, though, is that violence doesn’t go on that list. Sometimes we have no problem with it at all. This is a central point of this book—we don’t hate violence. We hate and fear the wrong kind of violence, violence in the wrong context. Because violence in the right context is different. We pay good money to watch it in a stadium, we teach our kids to fight back, we feel proud when, in creaky middle age, we manage a dirty hip-check in a weekend basketball game. Our conversations are filled with military metaphors—we rally the troops after our ideas get shot down. Our sports teams’ names celebrate violence—Warriors, Vikings, Lions, Tigers, and Bears. We even think this way about something as cerebral as chess —“Kasparov kept pressing for a murderous attack. Toward the end, Kasparov had to oppose threats of violence with more of the same.”1 We build theologies around violence, elect leaders who excel at it, and in the case of so many women, preferentially mate with champions of human combat. When it’s the “right” type of aggression, we love it. It is the ambiguity of violence, that we can pull a trigger as an act of hideous aggression or of self-sacrificing love, that is so challenging. As a result, violence will always be a part of the human experience that is profoundly hard to understand. This book explores the biology of violence, aggression, and competition— the behaviors and the impulses behind them, the acts of individuals, groups, and states, and when these are bad or good things. It is a book about the ways in which humans harm one another. But it is also a book about the ways in which people do the opposite. What does biology teach us about cooperation, affiliation, reconciliation, empathy, and altruism? The book has a number of personal roots. One is that, having had blessedly little personal exposure to violence in my life, the entire phenomenon scares the crap out of me. I think like an academic egghead, believing that if I write enough paragraphs about a scary subject, give enough lectures about it, it will give up and go away quietly. And if everyone took enough classes about the biology of violence and studied hard, we’d all be able to take a nap between the snoozing lion and lamb. Such is the delusional sense of efficacy of a professor. Then there’s the other personal root for this book. I am by nature majorly pessimistic. Give me any topic and I’ll find a way in which things will fall apart. Or turn out wonderfully and somehow, because of that, be poignant and sad. It’s a pain in the butt, especially to people stuck around me. And when I had kids, I realized that I needed to get ahold of this tendency big time. So I looked for evidence that things weren’t quite that bad. I started small, practicing on them— don’t cry, a T. rex would never come and eat you; of course Nemo’s daddy will find him. And as I’ve learned more about the subject of this book, there’s been an unexpected realization—the realms of humans harming one another are neither universal nor inevitable, and we’re getting some scientific insights into how to avoid them. My pessimistic self has a hard time admitting this, but there is room for optimism. THE APPROACH IN THIS BOOK Ibrain—and make my living as a combination neurobiologist—someone who studies the primatologist—someone who studies monkeys and apes. Therefore, this is a book that is rooted in science, specifically biology. And out of that come three key points. First, you can’t begin to understand things like aggression, competition, cooperation, and empathy without biology; I say this for the benefit of a certain breed of social scientist who finds biology to be irrelevant and a bit ideologically suspect when thinking about human social behavior. But just as important, second, you’re just as much up the creek if you rely only on biology; this is said for the benefit of a style of molecular fundamentalist who believes that the social sciences are destined to be consumed by “real” science. And as a third point, by the time you finish this book, you’ll see that it actually makes no sense to distinguish between aspects of a behavior that are “biological” and those that would be described as, say, “psychological” or “cultural.” Utterly intertwined. Understanding the biology of these human behaviors is obviously important. But unfortunately it is hellishly complicated.2 Now, if you were interested in the biology of, say, how migrating birds navigate, or in the mating reflex that occurs in female hamsters when they’re ovulating, this would be an easier task. But that’s not what we’re interested in. Instead, it’s human behavior, human social behavior, and in many cases abnormal human social behavior. And it is indeed a mess, a subject involving brain chemistry, hormones, sensory cues, prenatal environment, early experience, genes, both biological and cultural evolution, and ecological pressures, among other things. How are we supposed to make sense of all these factors in thinking about behavior? We tend to use a certain cognitive strategy when dealing with complex, multifaceted phenomena, in that we break down those separate facets into categories, into buckets of explanation. Suppose there’s a rooster standing next to you, and there’s a chicken across the street. The rooster gives a sexually solicitive gesture that is hot by chicken standards, and she promptly runs over to mate with him (I haven’t a clue if this is how it works, but let’s just suppose). And thus we have a key behavioral biological question—why did the chicken cross the road? And if you’re a psychoneuroendocrinologist, your answer would be “Because circulating estrogen levels in that chicken worked in a certain part of her brain to make her responsive to this male signaling,” and if you’re a bioengineer, the answer would be “Because the long bone in the leg of the chicken forms a fulcrum for her pelvis (or some such thing), allowing her to move forward rapidly,” and if you’re an evolutionary biologist, you’d say, “Because over the course of millions of years, chickens that responded to such gestures at a time that they were fertile left more copies of their genes, and thus this is now an innate behavior in chickens,” and so on, thinking in categories, in differing scientific disciplines of explanation. The goal of this book is to avoid such categorical thinking. Putting facts into nice cleanly demarcated buckets of explanation has its advantages—for example, it can help you remember facts better. But it can wreak havoc on your ability to think about those facts. This is because the boundaries between different categories are often arbitrary, but once some arbitrary boundary exists, we forget that it is arbitrary and get way too impressed with its importance. For example, the visual spectrum is a continuum of wavelengths from violet to red, and it is arbitrary where boundaries are put for different color names (for example, where we see a transition from “blue” to “green”); as proof of this, different languages arbitrarily split up the visual spectrum at different points in coming up with the words for different colors. Show someone two roughly similar colors. If the color-name boundary in that person’s language happens to fall between the two colors, the person will overestimate the difference between the two. If the colors fall in the same category, the opposite happens. In other words, when you think categorically, you have trouble seeing how similar or different two things are. If you pay lots of attention to where boundaries are, you pay less attention to complete pictures. Thus, the official intellectual goal of this book is to avoid using categorical buckets when thinking about the biology of some of our most complicated behaviors, even more complicated than chickens crossing roads. What’s the replacement? A behavior has just occurred. Why did it happen? Your first category of explanation is going to be a neurobiological one. What went on in that person’s brain a second before the behavior happened? Now pull out to a slightly larger field of vision, your next category of explanation, a little earlier in time. What sight, sound, or smell in the previous seconds to minutes triggered the nervous system to produce that behavior? On to the next explanatory category. What hormones acted hours to days earlier to change how responsive that individual was to the sensory stimuli that trigger the nervous system to produce the behavior? And by now you’ve increased your field of vision to be thinking about neurobiology and the sensory world of our environment and short-term endocrinology in trying to explain what happened. And you just keep expanding. What features of the environment in the prior weeks to years changed the structure and function of that person’s brain and thus changed how it responded to those hormones and environmental stimuli? Then you go further back to the childhood of the individual, their fetal environment, then their genetic makeup. And then you increase the view to encompass factors larger than that one individual—how has culture shaped the behavior of people living in that individual’s group?—what ecological factors helped shape that culture—expanding and expanding until considering events umpteen millennia ago and the evolution of that behavior. Okay, so this represents an improvement—it seems like instead of trying to explain all of behavior with a single discipline (e.g., “Everything can be explained with knowledge about this particular [take your pick:] hormone/gene/childhood event”), we’ll be thinking about a bunch of disciplinary buckets. But something subtler will be done, and this is the most important idea in the book: when you explain a behavior with one of these disciplines, you are implicitly invoking all the disciplines—any given type of explanation is the end product of the influences that preceded it. It has to work this way. If you say, “The behavior occurred because of the release of neurochemical Y in the brain,” you are also saying, “The behavior occurred because the heavy secretion of hormone X this morning increased the levels of neurochemical Y.” You’re also saying, “The behavior occurred because the environment in which that person was raised made her brain more likely to release neurochemical Y in response to certain types of stimuli.” And you’re also saying, “... because of the gene that codes for the particular version of neurochemical Y.” And if you’ve so much as whispered the word “gene,” you’re also saying, “... and because of the millennia of factors that shaped the evolution of that particular gene.” And so on. There are not different disciplinary buckets. Instead, each one is the end product of all the biological influences that came before it and will influence all the factors that follow it. Thus, it is impossible to conclude that a behavior is caused by a gene, a hormone, a childhood trauma, because the second you invoke one type of explanation, you are de facto invoking them all. No buckets. A “neurobiological” or “genetic” or “developmental” explanation for a behavior is just shorthand, an expository convenience for temporarily approaching the whole multifactorial arc from a particular perspective. Pretty impressive, huh? Actually, maybe not. Maybe I’m just pretentiously saying, “You have to think complexly about complex things.” Wow, what a revelation. And maybe what I’ve been tacitly setting up is this full-of-ourselves straw man of “Ooh, we’re going to think subtly. We won’t get suckered into simplistic answers, not like those chicken-crossing-the-road neurochemists and chicken evolutionary biologists and chicken psychoanalysts, all living in their own limited categorical buckets.” Obviously, scientists aren’t like that. They’re smart. They understand that they need to take lots of angles into account. Of necessity, their research may focus on a narrow subject, because there are limits to how much one person can obsess over. But of course they know that their particular categorical bucket isn’t the whole story. Maybe yes, maybe no. Consider the following quotes from some card- carrying scientists. The first: Give me a dozen healthy infants, well formed, and my own specified world to bring them up in and I’ll guarantee to take any one at random and train him to become any type of specialist I might select—doctor, lawyer, artist, merchant-chief and yes, even beggar-man thief, regardless of his talents, penchants, tendencies, abilities, vocations, and race of his ancestors.3 This was John Watson, a founder of behaviorism, writing around 1925. Behaviorism, with its notion that behavior is completely malleable, that it can be shaped into anything in the right environment, dominated American psychology in the midtwentieth century; we’ll return to behaviorism, and its considerable limitations. The point is that Watson was pathologically caught inside a bucket having to do with the environmental influences on development. “I’ll guarantee... to train him to become any type.” Yet we are not all born the same, with the same potential, regardless of how we are trained.*4 The next quote: Normal psychic life depends upon the good functioning of brain synapses, and mental disorders appear as a result of synaptic  derangements.... It is necessary to alter these synaptic adjustments and change the paths chosen by the impulses in their constant passage so as to modify the corresponding ideas and force thought into different channels.5 Alter synaptic adjustments. Sounds delicate. Yeah, right. These were the words of the Portuguese neurologist Egas Moniz, around the time he was awarded the Nobel Prize in 1949 for his development of frontal leukotomies. Here was an individual pathologically stuck in a bucket having to do with a crude version of the nervous system. Just tweak those microscopic synapses with a big ol’ ice pick (as was done once leukotomies, later renamed frontal lobotomies, became an assembly line operation). And a final quote: The immensely high reproduction rate in the moral imbecile has long been established.... Socially inferior human material is enabled... to penetrate and finally to annihilate the healthy nation. The selection for toughness, heroism, social utility... must be accomplished by some human institution if mankind, in default of selective factors, is not to be ruined by domestication-induced degeneracy. The racial idea as the basis of our state has already accomplished much in this respect. We must— and should—rely on the healthy feelings of our Best and charge them... with the extermination of elements of the population loaded with dregs.6 This was Konrad Lorenz, animal behaviorist, Nobel laureate, cofounder of the field of ethology (stay tuned), regular on nature TV programs.7 Grandfatherly Konrad, in his Austrian shorts and suspenders, being followed by his imprinted baby geese, was also a rabid Nazi propagandist. Lorenz joined the Nazi Party the instant Austrians were eligible, and joined the party’s Office of Race Policy, working to psychologically screen Poles of mixed Polish/German parentage, helping to determine which were sufficiently Germanized to be spared death. Here was a man pathologically mired in an imaginary bucket related to gross misinterpretations of what genes do. These were not obscure scientists producing fifth-rate science at Podunk U. These were among the most influential scientists of the twentieth century. They helped shape who and how we educate and our views on what social ills are fixable and when we shouldn’t bother. They enabled the destruction of the brains of people against their will. And they helped implement final solutions for problems that didn’t exist. It can be far more than a mere academic matter when a scientist thinks that human behavior can be entirely explained from only one perspective. OUR LIVES AS ANIMALS AND OUR HUMAN VERSATILITY AT BEING AGGRESSIVE S o we have a first intellectual challenge, which is to always think in this interdisciplinary way. The second challenge is to make sense of humans as apes, primates, mammals. Oh, that’s right, we’re a kind of animal. And it will be a challenge to figure out when we’re just like other animals and when we are utterly different. Some of the time we are indeed just like any other animal. When we’re scared, we secrete the same hormone as would some subordinate fish getting hassled by a bully. The biology of pleasure involves the same brain chemicals in us as in a capybara. Neurons from humans and brine shrimp work the same way. House two female rats together, and over the course of weeks they will synchronize their reproductive cycles so that they wind up ovulating within a few hours of each other. Try the same with two human females (as reported in some but not all studies), and something similar occurs. It’s called the Wellesley effect, first shown with roommates at all-women’s Wellesley College.8 And when it comes to violence, we can be just like some other apes—we pummel, we cudgel, we throw rocks, we kill with our bare hands. So some of the time an intellectual challenge is to assimilate how similar we can be to other species. In other cases the challenge is to appreciate how, though human physiology resembles that of other species, we use the physiology in novel ways. We activate the classical physiology of vigilance while watching a scary movie. We activate a stress response when thinking about mortality. We secrete hormones related to nurturing and social bonding, but in response to an adorable baby panda. And this certainly applies to aggression—we use the same muscles as does a male chimp attacking a sexual competitor, but we use them to harm someone because of their ideology. Finally, sometimes the only way to understand our humanness is to consider solely humans, because the things we do are unique. While a few other species have regular nonreproductive sex, we’re the only ones to talk afterward about how it was. We construct cultures premised on beliefs concerning the nature of life and can transmit those beliefs multigenerationally, even between two individuals separated by millennia—just consider that perennial best seller, the Bible. Consonant with that, we can harm by doing things as unprecedented as and no more physically taxing than pulling a trigger, or nodding consent, or looking the other way. We can be passive-aggressive, damn with faint praise, cut with scorn, express contempt with patronizing concern. All species are unique, but we are unique in some pretty unique ways. Here are two examples of just how strange and unique humans can be when they go about harming one another and caring for one another. The first example involves, well, my wife. So we’re in the minivan, our kids in the back, my wife driving. And this complete jerk cuts us off, almost causing an accident, and in a way that makes it clear that it wasn’t distractedness on his part, just sheer selfishness. My wife honks at him, and he flips us off. We’re livid, incensed. Asshole-where’s-the-cops-when-you-need-them, etc. And suddenly my wife announces that we’re going to follow him, make him a little nervous. I’m still furious, but this doesn’t strike me as the most prudent thing in the world. Nonetheless, my wife starts trailing him, right on his rear. After a few minutes the guy’s driving evasively, but my wife’s on him. Finally both cars stop at a red light, one that we know is a long one. Another car is stopped in front of the villain. He’s not going anywhere. Suddenly my wife grabs something from the front seat divider, opens her door, and says, “Now he’s going to be sorry.” I rouse myself feebly—“Uh, honey, do you really think this is such a goo—” But she’s out of the car, starts pounding on his window. I hurry over just in time to hear my wife say, “If you could do something that mean to another person, you probably need this,” in a venomous voice. She then flings something in the window. She returns to the car triumphant, just glorious. “What did you throw in there!?” She’s not talking yet. The light turns green, there’s no one behind us, and we just sit there. The thug’s car starts to blink a very sensible turn indicator, makes a slow turn, and heads down a side street into the dark at, like, five miles an hour. If it’s possible for a car to look ashamed, this car was doing it. “Honey, what did you throw in there, tell me?” She allows herself a small, malicious grin. “A grape lollipop.” I was awed by her savage passive-aggressiveness —“You’re such a mean, awful human that something must have gone really wrong in your childhood, and maybe this lollipop will help correct that just a little.” That guy was going to think twice before screwing with us again. I swelled with pride and love.  And the second example: In the mid-1960s, a rightist military coup overthrew the government of Indonesia, instituting the thirty-year dictatorship of Suharto known as the New Order. Following the coup, government-sponsored purges of communists, leftists, intellectuals, unionists, and ethnic Chinese left about a half million dead.9 Mass executions, torture, villages torched with inhabitants trapped inside. V. S. Naipaul, in his book Among the Believers: An Islamic Journey, describes hearing rumors while in Indonesia that when a paramilitary group would arrive to exterminate every person in some village, they would, incongruously, bring along a traditional gamelan orchestra. Eventually Naipaul encountered an unrepentant veteran of a massacre, and he asked him about the rumor. Yes, it is true. We would bring along gamelan musicians, singers, flutes, gongs, the whole shebang. Why? Why would you possibly do that? The man looked puzzled and gave what seemed to him a self- evident answer: “Well, to make it more beautiful.” Bamboo flutes, burning villages, the lollipop ballistics of maternal love. We have our work cut out for us, trying to understand the virtuosity with which we humans harm or care for one another, and how deeply intertwined the biology of the two can be.  One The Behavior W e have our strategy in place. A behavior has occurred—one that is reprehensible, or wonderful, or floating ambiguously in between. What occurred in the prior second that triggered the behavior? This is the province of the nervous system. What occurred in the prior seconds to minutes that triggered the nervous system to produce that behavior? This is the world of sensory stimuli, much of it sensed unconsciously. What occurred in the prior hours to days to change the sensitivity of the nervous system to such stimuli? Acute actions of hormones. And so on, all the way back to the evolutionary pressures played out over the prior millions of years that started the ball rolling. So we’re set. Except that when approaching this big sprawling mess of a subject, it is kind of incumbent upon you to first define your terms. Which is an unwelcome prospect. Here are some words of central importance to this book: aggression, violence, compassion, empathy, sympathy, competition, cooperation, altruism, envy, schadenfreude, spite, forgiveness, reconciliation, revenge, reciprocity, and (why not?) love. Flinging us into definitional quagmires. Why the difficulty? As emphasized in the introduction, one reason is that so many of these terms are the subject of ideological battles over the appropriation and distortions of their meanings.*1 Words pack power and these definitions are laden with values, often wildly idiosyncratic ones. Here’s an example, namely the ways I think about the word “competition”: (a) “competition”—your lab team races the Cambridge group to a discovery (exhilarating but embarrassing to admit to); (b) “competition”—playing pickup soccer (fine, as long as the best player shifts sides if the score becomes lopsided); (c) “competition”—your child’s teacher announces a prize for the best outlining-your-fingers Thanksgiving turkey drawing (silly and perhaps a red flag—if it keeps happening, maybe complain to the principal); (d) “competition”—whose deity is more worth killing for? (try to avoid). But the biggest reason for the definitional challenge was emphasized in the introduction—these terms mean different things to scientists living inside different disciplines. Is “aggression” about thought, emotion, or something done with muscles? Is “altruism” something that can be studied mathematically in various species, including bacteria, or are we discussing moral development in kids? And implicit in these different perspectives, disciplines have differing tendencies toward lumping and splitting—these scientists believe that behavior X consists of two different subtypes, whereas those scientists think it comes in seventeen flavors. Let’s examine this with respect to different types of “aggression.”2 Animal behaviorists dichotomize between offensive and defensive aggression, distinguishing between, say, the intruder and the resident of a territory; the biology underlying these two versions differs. Such scientists also distinguish between conspecific aggression (between members of the same species) and fighting off a predator. Meanwhile, criminologists distinguish between impulsive and premeditated aggression. Anthropologists care about differing levels of organization underlying aggression, distinguishing among warfare, clan vendettas, and homicide. Moreover, various disciplines distinguish between aggression that occurs reactively (in response to provocation) and spontaneous aggression, as well as between hot-blooded, emotional aggression and cold-blooded, instrumental aggression (e.g., “I want your spot to build my nest, so scram or I’ll peck your eyes out; this isn’t personal, though”).3 Then there’s another version of “This isn’t personal”—targeting someone just because they’re weak and you’re frustrated, stressed, or pained and need to displace some aggression. Such third- party aggression is ubiquitous—shock a rat and it’s likely to bite the smaller guy nearby; a beta-ranking male baboon loses a fight to the alpha, and he chases the omega male;* when unemployment rises, so do rates of domestic violence. Depressingly, as will be discussed in chapter 4, displacement aggression can decrease the perpetrator’s stress hormone levels; giving ulcers can help you avoid getting them. And of course there is the ghastly world of aggression that is neither reactive nor instrumental but is done for pleasure. Then there are specialized subtypes of aggression—maternal aggression, which often has a distinctive endocrinology. There’s the difference between aggression and ritualistic threats of aggression. For example, many primates have lower rates of actual aggression than of ritualized threats (such as displaying their canines). Similarly, aggression in Siamese fighting fish is mostly ritualistic.* Getting a definitional handle on the more positive terms isn’t easy either. There’s empathy versus sympathy, reconciliation versus forgiveness, and altruism versus “pathological altruism.”4 For a psychologist the last term might describe the empathic codependency of enabling a partner’s drug use. For a neuroscientist it describes a consequence of a type of damage to the frontal cortex—in economic games of shifting strategies, individuals with such damage fail to switch to less altruistic play when being repeatedly stabbed in the back by the other player, despite being able to verbalize the other player’s strategy. When it comes to the more positive behaviors, the most pervasive issue is one that ultimately transcends semantics—does pure altruism actually exist? Can you ever separate doing good from the expectation of reciprocity, public acclaim, self-esteem, or the promise of paradise? This plays out in a fascinating realm, as reported in Larissa MacFarquhar’s 2009 New Yorker piece “The Kindest Cut.”5 It concerns people who donate organs not to family members or close friends but to strangers. An act of seemingly pure altruism. But these Samaritans unnerve everyone, sowing suspicion and skepticism. Is she expecting to get paid secretly for her kidney? Is she that desperate for attention? Will she work her way into the recipient’s life and do a Fatal Attraction? What’s her deal? The piece suggests that these profound acts of goodness unnerve because of their detached, affectless nature. This speaks to an important point that runs through the book. As noted, we distinguish between hot-blooded and cold-blooded violence. We understand the former more, can see mitigating factors in it—consider the grieving, raging man who kills the killer of his child. And conversely, affectless violence seems horrifying and incomprehensible; this is the sociopathic contract killer, the Hannibal Lecter who kills without his heart rate nudging up a beat.*6 It’s why cold-blooded killing is a damning descriptor. Similarly, we expect that our best, most prosocial acts be warmhearted, filled with positive affect. Cold-blooded goodness seems oxymoronic, is unsettling. I was once at a conference of neuroscientists and all-star Buddhist monk meditators, the former studying what the brains of the latter did during meditation. One scientist asked one of the monks whether he ever stops meditating because his knees hurt from all that cross-leggedness. He answered, “Sometimes I’ll stop sooner than I planned, but not because it hurts; it’s not something I notice. It’s as an act of kindness to my knees.” “Whoa,” I thought, “these guys are from another planet.” A cool, commendable one, but another planet nonetheless. Crimes of passion and good acts of passion make the most sense to us (nevertheless, as we shall see, dispassionate kindness often has much to recommend it). Hot-blooded badness, warmhearted goodness, and the unnerving incongruity of the cold-blooded versions raise a key point, encapsulated in a quote from Elie Wiesel, the Nobel Peace Prize winner and concentration camp survivor: “The opposite of love is not hate; its opposite is indifference.” The biologies of strong love and strong hate are similar in many ways, as we’ll see. Which reminds us that we don’t hate aggression; we hate the wrong kind of aggression but love it in the right context. And conversely, in the wrong context our most laudable behaviors are anything but. The motoric features of our behaviors are less important and challenging to understand than the meaning behind our muscles’ actions. This is shown in a subtle study.7 Subjects in a brain scanner entered a virtual room where they encountered either an injured person in need of help or a menacing extraterrestrial; subjects could either bandage or shoot the individual. Pulling a trigger and applying a bandage are different behaviors. But they are similar, insofar as bandaging the injured person and shooting the alien are both the “right” things. And contemplating those two different versions of doing the right thing activated the same circuitry in the most context-savvy part of the brain, the prefrontal cortex. And thus those key terms that anchor this book are most difficult to define because of their profound context dependency. I will therefore group them in a way that reflects this. I won’t frame the behaviors to come as either pro- or antisocial—too cold-blooded for my expository tastes. Nor will they be labeled as “good” and “evil”—too hot-blooded and frothy. Instead, as our convenient shorthand for concepts that truly defy brevity, this book is about the biology of our best and worst behaviors.  Two One Second Before V arious muscles have moved, and a behavior has happened. Perhaps it is a good act: you’ve empathically touched the arm of a suffering person. Perhaps it is a foul act: you’ve pulled a trigger, targeting an innocent person. Perhaps it is a good act: you’ve pulled a trigger, drawing fire to save others. Perhaps it is a foul act: you’ve touched the arm of someone, starting a chain of libidinal events that betray a loved one. Acts that, as emphasized, are definable only by context. Thus, to ask the question that will begin this and the next eight chapters, why did that behavior occur? As this book’s starting point, we know that different disciplines produce different answers—because of some hormone; because of evolution; because of childhood experiences or genes or culture—and as the book’s central premise, these are utterly intertwined answers, none standing alone. But on the most proximal level, in this chapter we ask: What happened one second before the behavior that caused it to occur? This puts us in the realm of neurobiology, of understanding the brain that commanded those muscles. This chapter is one of the book’s anchors. The brain is the final common pathway, the conduit that mediates the influences of all the distal factors to be covered in the chapters to come. What happened an hour, a decade, a million years earlier? What happened were factors that impacted the brain and the behavior it produced. This chapter has two major challenges. The first is its god-awful length. Apologies; I’ve tried to be succinct and nontechnical, but this is foundational material that needs to be covered. Second, regardless of how nontechnical I’ve tried to be, the material can overwhelm someone with no background in neuroscience. To help with that, please wade through appendix 1 around now. — Now we ask: What crucial things happened in the second before that pro- or antisocial behavior occurred? Or, translated into neurobiology: What was going on with action potentials, neurotransmitters, and neural circuits in particular brain regions during that second? THREE METAPHORICAL (BUT NOT LITERAL) LAYERS W e start by considering the brain’s macroorganization, using a model proposed in the 1960s by the neuroscientist Paul MacLean.1 His “triune brain” model conceptualizes the brain as having three functional domains: Layer 1: An ancient part of the brain, at its base, found in species from humans to geckos. This layer mediates automatic, regulatory functions. If body temperature drops, this brain region senses it and commands muscles to shiver. If blood glucose levels plummet, that’s sensed here, generating hunger. If an injury occurs, a different loop initiates a stress response. Layer 2: A more recently evolved region that has expanded in mammals. MacLean conceptualized this layer as being about emotions, somewhat of a mammalian invention. If you see something gruesome and terrifying, this layer sends commands down to ancient layer 1, making you shiver with emotion. If you’re feeling sadly unloved, regions here prompt layer 1 to generate a craving for comfort food. If you’re a rodent and smell a cat, neurons here cause layer 1 to initiate a stress response. Layer 3: The recently evolved layer of neocortex sitting on the upper surface of the brain. Proportionately, primates devote more of their brain to this layer than do other species. Cognition, memory storage, sensory processing, abstractions, philosophy, navel contemplation. Read a scary passage of a book, and layer 3 signals layer 2 to make you feel frightened, prompting layer 1 to initiate shivering. See an ad for Oreos and feel a craving—layer 3 influences layers 2 and 1. Contemplate the fact that loved ones won’t live forever, or kids in refugee camps, or how the Na’vis’ home tree was destroyed by those jerk humans in Avatar (despite the fact that, wait, Na’vi aren’t real!), and layer 3 pulls layers 2 and 1 into the picture, and you feel sad and have the same sort of stress response that you’d have if you were fleeing a lion. Thus we’ve got the brain divided into three functional buckets, with the usual advantages and disadvantages of categorizing a continuum. The biggest disadvantage is how simplistic this is. For example:  a. Anatomically there is considerable overlap among the three layers (for example, one part of the cortex can best be thought of as part of layer 2; stay tuned). b. The flow of information and commands is not just top down, from layer 3 to 2 to 1. A weird, great example explored in chapter 15: if someone is holding a cold drink (temperature is processed in layer 1), they’re more likely to judge someone they meet as having a cold personality (layer 3). c. Automatic aspects of behavior (simplistically, the purview of layer 1), emotion (layer 2), and thought (layer 3) are not separable. d. The triune model leads one, erroneously, to think that evolution in effect slapped on each new layer without any changes occurring in the one(s) already there. Despite these drawbacks, which MacLean himself emphasized, this model will be a good organizing metaphor for us. THE LIMBIC SYSTEM T o make sense of our best and worst behaviors, automaticity, emotion, and cognition must all be considered; I arbitrarily start with layer 2 and its emphasis on emotion. Early-twentieth-century neuroscientists thought it obvious what layer 2 did. Take your standard-issue lab animal, a rat, and examine its brain. Right at the front would be these two gigantic lobes, the “olfactory bulbs” (one for each nostril), the primary receptive area for odors. Neuroscientists at the time asked what parts of the brain these gigantic rodent olfactory bulbs talked to (i.e., where they sent their axonal projections). Which brain regions were only a single synapse away from receiving olfactory information, which were two synapses, three, and so on? And it was layer 2 structures that received the first communiqués. Ah, everyone concluded, this part of the brain must process odors, and so it was termed the rhinencephalon—the nose brain. Meanwhile, in the thirties and forties, neuroscientists such as the young MacLean, James Papez, Paul Bucy, and Heinrich Klüver were starting to figure out what the layer 2 structures did. For example, if you lesion (i.e., destroy) layer 2 structures, this produces “Klüver-Bucy syndrome,” featuring abnormalities in sociality, especially in sexual and aggressive behaviors. They concluded that these structures, soon termed the “limbic system” (for obscure reasons), were about emotion. Rhinencephalon or limbic system? Olfaction or emotion? Pitched street battles ensued until someone pointed out the obvious—for a rat, emotion and olfaction are nearly synonymous, since nearly all the environmental stimuli that elicit emotions in a rodent are olfactory. Peace in our time. In a rodent, olfactory inputs are what the limbic system most depends on for emotional news of the world. In contrast, the primate limbic system is more informed by visual inputs. Limbic function is now recognized as central to the emotions that fuel our best and worst behaviors, and extensive research has uncovered the functions of its structures (e.g., the amygdala, hippocampus, septum, habenula, and mammillary bodies). There really aren’t “centers” in the brain “for” particular behaviors. This is particularly the case with the limbic system and emotion. There is indeed a sub- subregion of the motor cortex that approximates being the “center” for making your left pinkie bend; other regions have “center”-ish roles in regulating breathing or body temperature. But there sure aren’t centers for feeling pissy or horny, for feeling bittersweet nostalgia or warm protectiveness tinged with contempt, or for that what-is-that-thing-called-love feeling. No surprise, then, that the circuitry connecting various limbic structures is immensely complex. The Autonomic Nervous System and the Ancient Core Regions of the Brain The limbic system’s regions form complex circuits of excitation and inhibition. It’s easier to understand this by appreciating the deeply held desire of every limbic structure—to influence what the hypothalamus does. Why? Because of its importance. The hypothalamus, a limbic structure, is the interface between layers 1 and 2, between core regulatory and emotional parts of the brain. Consistent with that, the hypothalamus gets massive inputs from limbic layer 2 structures but disproportionately sends projections to layer 1 regions. These are the evolutionarily ancient midbrain and brain stem, which regulate automatic reactions throughout the body. For a reptile such automatic regulation is straightforward. If muscles are working hard, this is sensed by neurons throughout the body that send signals up the spine to layer 1 regions, resulting in signals back down the spine that increase heart rate and blood pressure; the result is more oxygen and glucose for the muscles. Gorge on food, and stomach walls distend; neurons embedded there sense this and pass on the news, and soon blood vessels in the gut dilate, increasing blood flow and facilitating digestion. Too warm? Blood is sent to the body’s surface to dissipate heat. — All of this is automatic, or “autonomic.” And thus the midbrain and brain-stem regions, along with their projections down the spine and out to the body, are collectively termed the “autonomic nervous system.”* And where does the hypothalamus come in? It’s the means by which the limbic system influences autonomic function, how layer 2 talks to layer 1. Have a full bladder with its muscle walls distended, and midbrain/brain-stem circuitry votes for urinating. Be exposed to something sufficiently terrifying, and limbic structures, via the hypothalamus, persuade the midbrain and brain stem to do the same. This is how emotions change bodily functions, why limbic roads eventually lead to the hypothalamus.* The autonomic nervous system has two parts—the sympathetic and parasympathetic nervous systems, with fairly opposite functions. The sympathetic nervous system (SNS) mediates the body’s response to arousing circumstances, for example, producing the famed “fight or flight” stress response. To use the feeble joke told to first-year medical students, the SNS mediates the “four Fs—fear, fight, flight, and sex.” Particular midbrain/brain- stem nuclei send long SNS projections down the spine and on to outposts throughout the body, where the axon terminals release the neurotransmitter norepinephrine. There’s one exception that makes the SNS more familiar. In the adrenal gland, instead of norepinephrine (aka noradrenaline) being released, it’s epinephrine (aka the famous adrenaline).* Meanwhile, the parasympathetic nervous system (PNS) arises from different midbrain/brain-stem nuclei that project down the spine to the body. In contrast to the SNS and the four Fs, the PNS is about calm, vegetative states. The SNS speeds up the heart; the PNS slows it down. The PNS promotes digestion; the SNS inhibits it (which makes sense—if you’re running for your life, avoiding being someone’s lunch, don’t waste energy digesting breakfast).* And as we will see chapter 14, if seeing someone in pain activates your SNS, you’re likely to be preoccupied with your own distress instead of helping; turn on the PNS, and it’s the opposite. Given that the SNS and PNS do opposite things, the PNS is obviously going to be releasing a different neurotransmitter from its axon terminals—acetylcholine.* There is a second, equally important way in which emotion influences the body. Specifically, the hypothalamus also regulates the release of many hormones; this is covered in chapter 4. — So the limbic system indirectly regulates autonomic function and hormone release. What does this have to do with behavior? Plenty—because the autonomic and hormonal states of the body feed back to the brain, influencing behavior (typically unconsciously).* Stay tuned for more in chapters 3 and 4. The Interface Between the Limbic System and the Cortex Time to add the cortex. As noted, this is the brain’s upper surface (its name comes from the Latin cortic, meaning “tree bark”) and is the newest part of the brain. The cortex is the gleaming, logical, analytical crown jewel of layer 3. Most sensory information flows there to be decoded. It’s where muscles are commanded to move, where language is comprehended and produced, where memories are stored, where spatial and mathematical skills reside, where executive decisions are made. It floats above the limbic system, supporting philosophers since at least Descartes who have emphasized the dichotomy between thought and emotion. Of course, that’s all wrong, as shown by the temperature of a cup— something processed in the hypothalamus—altering assessment of the coldness of someone’s personality. Emotions filter the nature and accuracy of what is remembered. Stroke damage to certain cortical regions blocks the ability to speak; some sufferers reroute the cerebral world of speech through emotive, limbic detours—they can sing what they want to say. The cortex and limbic system are not separate, as scads of axonal projections course between the two. Crucially, those projections are bidirectional—the limbic system talks to the cortex, rather than merely being reined in by it. The false dichotomy between thought and feeling is presented in the classic Descartes’ Error, by the neurologist Antonio Damasio of the University of Southern California; his work is discussed later.2 While the hypothalamus dwells at the interface of layers 1 and 2, it is the incredibly interesting frontal cortex that is the interface between layers 2 and 3. Key insight into the frontal cortex was provided in the 1960s by a giant of neuroscience, Walle Nauta of MIT.*3 Nauta studied what brain regions sent axons to the frontal cortex and what regions got axons from it. And the frontal cortex was bidirectionally enmeshed with the limbic system, leading him to propose that the frontal cortex is a quasi member of the limbic system. Naturally, everyone thought him daft. The frontal cortex was the most recently evolved part of the very highbrow cortex—the only reason why the frontal cortex would ever go slumming into the limbic system would be to preach honest labor and Christian temperance to the urchins there. Naturally, Nauta was right. In different circumstances the frontal cortex and limbic system stimulate or inhibit each other, collaborate and coordinate, or bicker and work at cross-purposes. It really is an honorary member of the limbic system. And the interactions between the frontal cortex and (other) limbic structures are at the core of much of this book. Two more details. First, the cortex is not a smooth surface but instead is folded into convolutions. The convolutions form a superstructure of four separate lobes: the temporal, parietal, occipital, and frontal, each with different functions.  Brain Lateralization Analytical Intuitive thought thought Holistic Detail-oriented perception perception Random Ordered sequencing sequencing Emotional Rational thought thought Verbal Nonverbal Cautious Adventurous Planning Impulse Math/science Creative Logic writing/art Right-field Imagination vision Left-field vision  Right-side motor Left-side motor skills skills Second, brains obviously have left and right sides, or “hemispheres,” that roughly mirror each other. Thus, except for the relatively few midline structures, brain regions come in pairs (a left and right amygdala, hippocampus, temporal lobe, and so on). Functions are often lateralized, such that the left and right hippocampi, for example, have different but related functions. The greatest lateralization occurs in the cortex; the left hemisphere is analytical, the right more involved in intuition and creativity. These contrasts have caught the public fancy, with cortical lateralization exaggerated by many to an absurd extent, where “left brain”–edness has the connotation of anal-retentive bean counting and “right brain”–edness is about making mandalas or singing with whales. In fact the functional differences between the hemispheres are generally subtle, and I’m mostly ignoring lateralization. We’re now ready to examine the brain regions most central to this book, namely the amygdala, the frontal cortex, and the mesolimbic/mesocortical dopamine system (discussion of other bit-player regions will be subsumed under the headings for these three). We start with the one arguably most central to our worst behaviors. THE AMYGDALA T he amygdala* is the archetypal limbic structure, sitting under the cortex in the temporal lobe. It is central to mediating aggression, along with other behaviors that tell us tons about aggression. A First Pass at the Amygdala and Aggression The evidence for the amygdala’s role in aggression is extensive, based on research approaches that will become familiar. First there’s the correlative “recording” approach. Stick recording electrodes into numerous species’ amygdalae* and see when neurons there have action potentials; this turns out to be when the animal is being aggressive.* In a related approach, determine which brain regions consume extra oxygen or glucose, or synthesize certain activity-related proteins, during aggression—the amygdala tops the list. Moving beyond mere correlation, if you lesion the amygdala in an animal, rates of aggression decline. The same occurs transiently when you temporarily silence the amygdala by injecting Novocain into it. Conversely, implanting electrodes that stimulate neurons there, or spritzing in excitatory neurotransmitters (stay tuned), triggers aggression.4 Show human subjects pictures that provoke anger, and the amygdala activates (as shown with neuroimaging). Sticking an electrode in someone’s amygdala and stimulating it (as is done before certain types of neurosurgery) produces rage. The most convincing data concern rare humans with damage restricted to the amygdala, either due to a type of encephalitis or a congenital disorder called Urbach-Wiethe disease, or where the amygdala was surgically destroyed to control severe, drug-resistant seizures originating there.5 Such individuals are impaired in detecting angry facial expressions (while being fine at recognizing other emotional states—stay tuned). And what does amygdala damage do to aggressive behavior? This was studied in humans where amygdalotomies were done not to control seizures but to control aggression. Such psychosurgery provoked fiery controversy in the 1970s. And I don’t mean scientists not saying hello to each other at conferences. I mean a major public shit storm. The issue raised bioethical lightning rods: What counted as pathological aggression? Who decided? What other interventions had been tried unsuccessfully? Were some types of hyperaggressive individuals more likely to go under the knife than others? What constituted a cure?6 Most of these cases concerned rare epileptics where seizure onset was associated with uncontrollable aggression, and where the goal was to contain that behavior (these papers had titles such as “Clinical and physiological effects of stereotaxic bilateral amygdalotomy for intractable aggression”). The fecal hurricane concerned the involuntary lopping out of the amygdala in people without epilepsy but with a history of severe aggression. Well, doing this could be profoundly helpful. Or Orwellian. This is a long, dark story and I will save it for another time. Did destruction of the human amygdala lessen aggression? Pretty clearly so, when violence was a reflexive, inchoate outburst preceding a seizure. But with surgery done solely to control behavior, the answer is, er, maybe—the heterogeneity of patients and surgical approaches, the lack of modern neuroimaging to pinpoint exactly which parts of the amygdala were destroyed in each individual, and the imprecision in the behavioral data (with papers reporting from 33 to 100 percent “success” rates) make things inconclusive. The procedure has almost entirely fallen out of practice. The amygdala/aggression link pops up in two notorious cases of violence. The first concerns Ulrike Meinhof, a founder in 1968 of the Red Army Faction (aka the Baader-Meinhof Gang), a terrorist group responsible for bombings and bank robberies in West Germany. Meinhof had a conventional earlier life as a journalist before becoming violently radicalized. During her 1976 murder trial, she was found hanged in her jail cell (suicide or murder? still unclear). In 1962 Meinhof had had a benign brain tumor surgically removed; the 1976 autopsy showed that remnants of the tumor and surgical scar tissue impinged on her amygdala.7 A second case concerns Charles Whitman, the 1966 “Texas Tower” sniper who, after killing his wife and mother, opened fire atop a tower at the University of Texas in Austin, killing sixteen and wounding thirty-two, one of the first school massacres. Whitman was literally an Eagle Scout and childhood choirboy, a happily married engineering major with an IQ in the 99th percentile. In the prior year he had seen doctors, complaining of severe headaches and violent impulses (e.g., to shoot people from the campus tower). He left notes by the bodies of his wife and his mother, proclaiming love and puzzlement at his actions: “I cannot rationaly [sic] pinpoint any specific reason for [killing her],” and “let there be no doubt in your mind that I loved this woman with all my heart.” His suicide note requested an autopsy of his brain, and that any money he had be given to a mental health foundation. The autopsy proved his intuition correct—Whitman had a glioblastoma tumor pressing on his amygdala. Did Whitman’s tumor “cause” his violence? Probably not in a strict “amygdaloid tumor = murderer” sense, as he had risk factors that interacted with his neurological issues. Whitman grew up being beaten by his father and watching his mother and siblings experience the same. This choirboy Eagle Scout had repeatedly physically abused his wife and had been court-martialed as a Marine for physically threatening another soldier.* And, perhaps indicative of a thread running through the family, his brother was murdered at age twenty-four during a bar fight.8 A Whole Other Domain of Amygdaloid Function to the Center Stage Thus considerable evidence implicates the amygdala in aggression. But if you asked amygdala experts what behavior their favorite brain structure brings to mind, “aggression” wouldn’t top their list. It would be fear and anxiety.9 Crucially, the brain region most involved in feeling afraid and anxious is most involved in generating aggression. The amygdala/fear link is based on evidence similar to that supporting the amygdala/aggression link.10 In lab animals this has involved lesioning the structure, detecting activity in its neurons with “recording electrodes,” electrically stimulating it, or manipulating genes in it. All suggest a key role for the amygdala in perceiving fear-provoking stimuli and in expressing fear. Moreover, fear activates the amygdala in humans, with more activation predicting more behavioral signs of fear. In one study subjects in a brain scanner played a Ms. Pac-Man–from–hell video game where they were pursued in a maze by a dot; if caught, they’d be shocked.11 When people were evading the dot, the amygdala was silent. However, its activity increased as the dot approached; the stronger the shocks, the farther away the dot would be when first activating the amygdala, the stronger the activation, and the larger the self-reported feeling of panic. In another study subjects waited an unknown length of time to receive a shock.12 This lack of predictability and control was so aversive that many chose to receive a stronger shock immediately. And in the others the period of anticipatory dread increasingly activated the amygdala. Thus the human amygdala preferentially responds to fear-evoking stimuli, even stimuli so fleeting as to be below conscious detection. Powerful support for an amygdaloid role in fear processing comes from post- traumatic stress disorder (PTSD). In PTSD sufferers the amygdala is overreactive to mildly fearful stimuli and is slow in calming down after being activated.13 Moreover, the amygdala expands in size with long-term PTSD. This role of stress in this expansion will be covered in chapter 4. The amygdala is also involved in the expression of anxiety.14 Take a deck of cards—half are black, half are red; how much would you wager that the top card is red? That’s about risk. Here’s a deck of cards—at least one is black, at least one is red; how much would you wager that the top card is red? That’s about ambiguity. The circumstances carry identical probabilities, but people are made more anxious by the second scenario and activate the amygdala more. The amygdala is particularly sensitive to unsettling circumstances that are social. A high-ranking male rhesus monkey is in a sexual consortship with a female; in one condition the female is placed in another room, where the male can see her. In the second she’s in the other room along with a rival of the male. No surprise, that situation activates the amygdala. Is that about aggression or anxiety? Seemingly the latter—the extent of activation did not correlate with the amount of aggressive behaviors and vocalizations the male made, or the amount of testosterone secreted. Instead, it correlated with the extent of anxiety displayed (e.g., teeth chattering, or self-scratching). The amygdala is linked to social uncertainty in other ways. In one neuroimaging study, a subject would participate in a competitive game against a group of other players; outcomes were rigged so that the subject would wind up in the middle of the rankings.15 Experimenters then manipulated game outcomes so that subjects’ rankings either remained stable or fluctuated wildly. Stable rankings activated parts of the frontal cortex that we’ll soon consider. Instability activated the frontal cortex plus the amygdala. Being unsure of your place is unsettling.  Another study explored the neurobiology of conforming.16 To simplify, a subject is part of a group (where, secretly, the rest are confederates); they are shown “X,” then asked, “What did you see?” Everyone else says “Y.” Does the subject lie and say “Y” also? Often. Subjects who stuck to their guns with “X” showed amygdala activation. Finally, activating specific circuits within the amygdala in mice turns anxiety on and off; activating others made mice unable to distinguish between safe and anxiety-producing settings.*17 The amygdala also helps mediate both innate and learned fear.18 The core of innate fear (aka a phobia) is that you don’t have to learn by trial and error that something is aversive. For example, a rat born in a lab, who has interacted only with other rats and grad students, instinctually fears and avoids the smell of cats. While different phobias activate somewhat different brain circuitry (for example, dentist phobia involves the cortex more than does snake phobia), they all activate the amygdala. Such innate fear contrasts with things we learn to fear—a bad neighborhood, a letter from the IRS. The dichotomy between innate and learned fear is actually a bit fuzzy.19 Everyone knows that humans are innately afraid of snakes and spiders. But some people keep them as pets, give them cute names.* Instead of inevitable fear, we show “prepared learning”—learning to be afraid of snakes and spiders more readily than of pandas or beagles. The same occurs in other primates. For example, lab monkeys who have never encountered snakes (or artificial flowers) can be conditioned to fear the former more readily than the latter. As we’ll see in the next chapter, humans show prepared learning, being predisposed to be conditioned to fear people with a certain type of appearance. The fuzzy distinction between innate and learned fear maps nicely onto the amygdala’s structure. The evolutionarily ancient central amygdala plays a key role in innate fears. Surrounding it is the basolateral amygdala (BLA), which is more recently evolved and somewhat resembles the fancy, modern cortex. It’s the BLA that learns fear and then sends the news to the central amygdala. Joseph LeDoux at New York University has shown how the BLA learns fear.*20 Expose a rat to an innate trigger of fear—a shock. When this “unconditioned stimulus” occurs, the central amygdala activates, stress hormones are secreted, the sympathetic nervous system mobilizes, and, as a clear end point, the rat freezes in place—“What was that? What do I do?” Now do some conditioning. Before each shock, expose the rat to a stimulus that normally does not evoke fear, such as a tone. And with repeated coupling of the tone (the conditioned stimulus) with the shock (the unconditioned one), fear conditioning occurs—the sound of the tone alone elicits freezing, stress hormone release, and so on.* LeDoux and others have shown how auditory information about the tone stimulates BLA neurons. At first, activation of those neurons is irrelevant to the central amygdala (whose neurons are destined to activate following the shock). But with repeated coupling of tone with shock, there is remapping and those BLA neurons acquire the means to activate the central amygdala.* BLA neurons that respond to the tone only once conditioning has occurred would also have responded if conditioning instead had been to a light. In other words, these neurons respond to the meaning of the stimulus, rather than to its specific modality. Moreover, if you electrically stimulate them, rats are easier to fear-condition; you’ve lowered the threshold for this association to be made. And if you electrically stimulate the auditory sensory input at the same time as shocks (i.e., there’s no tone, just activation of the pathway that normally carries news of the tone to the amygdala), you cause fear conditioning to a tone. You’ve engineered the learning of a false fear. There are synaptic changes as well. Once conditioning to a tone has occurred, the synapses coupling the BLA and central nucleus neurons have become more excitable; how this occurs is understood at the level of changes in the amount of receptors for excitatory neurotransmitters in dendritic spines in these circuits.* Furthermore, conditioning increases levels of “growth factors,” which prompt the growth of new connections between BLA and central amygdala neurons; some of the genes involved have even been identified. We’ve now got learning to be afraid under our belts.*21 Now conditions change—the tone still occurs now and then, but no more shock. Gradually the conditioned fear response abates. How does “fear extinction” occur? How do we learn that this person wasn’t so scary after all, that different doesn’t necessarily equal frightening? Recall how a subset of BLA neurons respond to the tone only once conditioning has occurred. Another population does the opposite, responding to the tone once it’s no longer signaling shock (logically, the two populations of neurons inhibit each other). Where do these “Ohhh, the tone isn’t scary anymore” neurons get inputs from? The frontal cortex. When we stop fearing something, it isn’t because some amygdaloid neurons have lost their excitability. We don’t passively forget that something is scary. We actively learn that it isn’t anymore.*  The amygdala also plays a logical role in social and emotional decision making. In the Ultimatum Game, an economic game involving two players, the first makes an offer as to how to divide a pot of money, which the other player either accepts or rejects.22 If the latter, neither gets anything. Research shows that rejecting an offer is an emotional decision, triggered by anger at a lousy offer and the desire to punish. The more the amygdala activation in the second player after an offer, the more likely the rejection. People with damaged amygdalae are atypically generous in the Ultimatum Game and don’t increase rejection rates if they start receiving unfair offers. Why? These individuals understand the rules and can give sound, strategic advice to other players. Moreover, they use the same strategies as control subjects in a nonsocial version of the game, when believing the other player is a computer. And they don’t have a particularly long view, undistracted by the amygdala’s emotional tumult, reasoning that their noncontingent generosity will induce reciprocity and pay off in the long run. When asked, they anticipate the same levels of reciprocity as do controls. Instead, these findings suggest that the amygdala injects implicit distrust and vigilance into social decision making.23 All thanks to learning. In the words of the authors of the study, “The generosity in the trust game of our BLA-damaged subjects might be considered pathological altruism, in the sense that inborn altruistic behaviors have not, due to BLA damage, been un-learned through negative social experience.” In other words, the default state is to trust, and what the amygdala does is learn vigilance and distrust. Unexpectedly, the amygdala and one of its hypothalamic targets also play a role in male sexual motivation (other hypothalamic nuclei are central to male sexual performance)* but not female.* What’s that about? One neuroimaging study sheds some light. “Young heterosexual men” looked at pictures of attractive women (versus, as a control, of attractive men). Passively observing the pictures activated the reward circuitry just alluded to. In contrast, working to see the pictures—by repeatedly pressing a button—also activated the amygdala. Similarly, other studies show that the amygdala is most responsive to positive stimuli when the value of the reward is shifting. Moreover, some BLA neurons that respond in that circumstance also respond when the severity of something aversive is shifting—these neurons are paying attention to change, independent of direction. For them, “the amount of reward is changing” and “the amount of punishment is changing” are the same. Studies like these clarify that the amygdala isn’t about the pleasure of experiencing pleasure. It’s about the uncertain, unsettled yearning for a potential pleasure, the anxiety and fear and anger that the reward may be smaller than anticipated, or may not even happen. It’s about how many of our pleasures and our pursuits of them contain a corrosive vein of disease.*24 The Amygdala as Part of Networks in the Brain Now that we know about the subparts of the amygdala, it’s informative to consider its extrinsic connections—i.e., what parts of the brain send projection to it, and what parts does it project to?25 SOME INPUTS TO THE AMYGDALA Sensory inputs. For starters, the amygdala, specifically the BLA, gets projections from all the sensory systems.26 How else can you get terrified by the shark’s theme music in Jaws? Normally, sensory information from various modalities (eyes, ears, skin...) courses into the brain, reaching the appropriate cortical region (visual cortex, auditory cortex, tactile cortex...) for processing. For example, the visual cortex would engage layers and layers of neurons to turn pixels of retinal stimulation into recognizable images before it can scream to the amygdala, “It’s a gun!” Importantly, some sensory information entering the brain takes a shortcut, bypassing the cortex and going directly to the amygdala. Thus the amygdala can be informed about something scary before the cortex has a clue. Moreover, thanks to the extreme excitability of this pathway, the amygdala can respond to stimuli that are too fleeting or faint for the cortex to note. Additionally, the shortcut projections form stronger, more excitable synapses in the BLA than do the ones from the sensory cortex; emotional arousal enhances fear conditioning through this pathway. This shortcut’s power is shown in the case of a man with stroke damage to his visual cortex, producing “cortical blindness.” While unable to process most visual information, he still recognized emotional facial expressions via the shortcut.* Crucially, while sensory information reaches the amygdala rapidly by this shortcut, it isn’t terribly accurate (since, after all, accuracy is what the cortex supplies). As we’ll see in the next chapter, this produces tragic circumstances where, say, the amygdala decides it’s seeing a handgun before the visual cortex can report that it’s actually a cell phone.  Information about pain. The amygdala receives news of that reliable trigger of fear and aggression, namely pain.27 This is mediated by projections from an ancient, core brain structure, the “periaqueductal gray” (PAG); stimulation of the PAG can evoke panic attacks, and it is enlarged in people with chronic panic attacks. Reflecting the amygdala’s roles in vigilance, uncertainty, anxiety, and fear, it’s unpredictable pain, rather than pain itself, that activates the amygdala. Pain (and the amygdala’s response to it) is all about context. Disgust of all stripes. The amygdala also receives a hugely interesting projection from the “insular cortex,” an honorary part of the prefrontal cortex, which we will consider at length in later chapters.28 If you (or any other mammal) bite into rancid food, the insular cortex lights up, causing you to spit it out, gag, feel nauseated, make a revolted facial expression—the insular cortex processes gustatory disgust. Ditto for disgusting smells. Remarkably, humans also activate it by thinking about something morally disgusting—social norm violations or individuals who are typically stigmatized in society. And in that circumstance its activation drives that of the amygdala. Someone does something lousy and selfish to you in a game, and the extent of insular and amygdaloid activation predicts how much outrage you feel and how much revenge you take. This is all about sociality—the insula and amygdala don’t activate if it’s a computer that has stabbed you in the back. The insula activates when we eat a cockroach or imagine doing so. And the insula and amygdala activate when we think of the neighboring tribe as loathsome cockroaches. As we’ll see, this is central to how our brains process “us and them.” And finally, the amygdala gets tons of inputs from the frontal cortex. Much more to come. SOME OUTPUTS FROM THE AMYGDALA As we’ll see, the amygdala talks to many of the regions Bidirectional connections. that talk to it, including the frontal cortex, insula, periaqueductal gray, and sensory projections, modulating their sensitivity. The amygdala/hippocampus interface. Naturally, the amygdala talks to other limbic structures, including the hippocampus. As reviewed, typically the amygdala learns fear and the hippocampus learns detached, dispassionate facts. But at times of extreme fear, the amygdala pulls the hippocampus into a type of fear learning.29  Back to the rat undergoing fear conditioning. When it’s in cage A, a tone is followed by a shock. But in cage B, the tone isn’t. This produces context- dependent conditioning—the tone causes fearful freezing in cage A but not in cage B. The amygdala learns the stimulus cue—the tone—while the hippocampus learns about the contexts of cage A versus B. The coupled learning between amygdala and hippocampus is very focalized—we all remember the view of the plane hitting the second World Trade Center tower, but not whether there were clouds in the background. The hippocampus decides whether a factoid is worth filing away, depending on whether the amygdala has gotten worked up over it. Moreover, the coupling can rescale. Suppose someone robs you at gunpoint in an alley in a bad part of town. Afterward, depending on the circumstance, the gun can be the cue and the alley the context, or the alley is the cue and the bad part of town the context. Motor outputs. There’s a second shortcut regarding the amygdala, specifically when it’s talking to motor neurons that command movement.30 Logically, when the amygdala wants to mobilize a behavior—say, fleeing—it talks to the frontal cortex, seeking its executive approval. But if sufficiently aroused, the amygdala talks directly to subcortical, reflexive motor pathways. Again, there’s a trade-off —increased speed by bypassing the cortex, but decreased accuracy. Thus the input shortcut may prompt you to see the cell phone as a gun. And the output shortcut may prompt you to pull a trigger before you consciously mean to. Arousal. Ultimately, amygdala outputs are mostly about setting off alarms throughout the brain and body. As we saw, the core of the amygdala is the central amygdala.31 Axonal projections from there go to an amygdala-ish structure nearby called the bed nucleus of the stria terminalis (BNST). The BNST, in turn, projects to parts of the hypothalamus that initiate the hormonal stress response (see chapter 4), as well as to midbrain and brain-stem sites that activate the sympathetic nervous system and inhibit the parasympathetic nervous system. Something emotionally arousing occurs, layer 2 limbic amygdala signals layer 1 regions, and heart rate and blood pressure soar.* The amygdala also activates a brain-stem structure called the locus coeruleus, akin to the brain’s own sympathetic nervous system.32 It sends norepinephrine-releasing projections throughout the brain, particularly the cortex. If the locus coeruleus is drowsy and silent, so are you. If it’s moderately activated, you’re alert. And if it’s firing like gangbusters, thanks to inputs from an aroused amygdala, all neuronal hands are on deck.  The amygdala’s projection pattern raises an important point.33 When is the sympathetic nervous system going full blast? During fear, flight, fight, and sex. Or if you’ve won the lottery, are happily sprinting down a soccer field, or have just solved Fermat’s theorem (if you’re that kind of person). Reflecting this, about a quarter of neurons in one hypothalamic nucleus are involved in both sexual behavior and, when stimulated at a higher intensity, aggressive behavior in male mice. This has two implications. Both sex and aggression activate the sympathetic nervous system, which in turn can influence behavior—people feel differently about things if, say, their heart is racing versus beating slowly. Does this mean that the pattern of your autonomic arousal influences what you feel? Not really. But autonomic feedback influences the intensity of what is felt. More on this in the next chapter. The second consequence reflects a core idea of this book. Your heart does roughly the same thing whether you are in a murderous rage or having an orgasm. Again, the opposite of love is not hate, it’s indifference. — This concludes our overview of the amygdala. Amid the jargon and complexity, the most important theme is the amygdala’s dual role in both aggression and facets of fear and anxiety. Fear and aggression are not inevitably intertwined— not all fear causes aggression, and not all aggression is rooted in fear. Fear typically increases aggression only in those already prone to it; among the subordinate who lack the option of expressing aggression safely, fear does the opposite. The dissociation between fear and aggression is evident in violent psychopaths, who are the antithesis of fearful—both physiologically and subjectively they are less reactive to pain; their amygdalae are relatively unresponsive to typical fear-evoking stimuli and are smaller than normal.34 This fits with the picture of psychopathic violence; it is not done in aroused reaction to provocation. Instead, it is purely instrumental, using others as a means to an end with emotionless, remorseless, reptilian indifference. Thus, fear and violence are not always connected at the hip. But a connection is likely when the aggression evoked is reactive, frenzied, and flecked with spittle. In a world in which no amygdaloid neuron need be afraid and instead can sit under its vine and fig tree, the world is very likely to be a more peaceful place.*  — We now move to the second of the three brain regions we’re considering in detail. THE FRONTAL CORTEX I ’ve spent decades studying the hippocampus. It’s been good to me; I’d like to think I’ve been the same in return. Yet I think I might have made the wrong choice back then—maybe I should have studied the frontal cortex all these years. Because it’s the most interesting part of the brain. What does the frontal cortex do? Its list of expertise includes working memory, executive function (organizing knowledge strategically, and then initiating an action based on an executive decision), gratification postponement, long-term planning, regulation of emotions, and reining in impulsivity.35 This is a sprawling portfolio. I will group these varied functions under a single definition, pertinent to every page of this book: the frontal cortex makes you do the harder thing when it’s the right thing to do. To start, here are some important features of the frontal cortex: It’s the most recently evolved brain region, not approaching full splendor until the emergence of primates; a disproportionate percentage of genes unique to primates are active in the frontal cortex. Moreover, such gene expression patterns are highly individuated, with greater interindividual variability than average levels of whole-brain differences between humans and chimps. The human frontal cortex is more complexly wired than in other apes and, by some definitions as to its boundaries, proportionately bigger as well.36 The frontal cortex is the last brain region to fully mature, with the most evolutionarily recent subparts the very last. Amazingly, it’s not fully online until people are in their midtwenties. You’d better bet this factoid will be relevant to the chapter about adolescence.  Finally, the frontal cortex has a unique cell type. In general, the human brain isn’t unique because we’ve evolved unique types of neurons, neurotransmitters, enzymes, and so on. Human and fly neurons are remarkably similar; the uniqueness is quantitative—for every fly neuron, we have a gazillion more neurons and a bazillion more connections.37 The sole exception is an obscure type of neuron with a distinctive shape and pattern of wiring, called von Economo neurons (aka spindle neurons). At first they seemed to be unique to humans, but we’ve now found them in other primates, whales, dolphins, and elephants.* That’s an all-star team of socially complex species. Moreover, the few von Economo neurons occur only in two subregions of the frontal cortex, as shown by John Allman at Caltech. One we’ve heard about already—the insula, with its role in gustatory and moral disgust. The second is an equally interesting area called the anterior cingulate. To give a hint (with more to come), it’s central to empathy. So from the standpoint of evolution, size, complexity, development, genetics, and neuron type, the frontal cortex is distinctive, with the human version the most unique. The Subregions of the Frontal Cortex Frontal cortical anatomy is hellishly complicated, and there are debates as to whether some parts of the primate frontal cortex even exist in “simpler” species. Nonetheless, there are some useful broad themes. In the very front is the prefrontal cortex (PFC), the newest part of the frontal cortex. As noted, the frontal cortex is central to executive function. To quote George W. Bush, within the frontal cortex, it’s the PFC that is “the decider.” Most broadly, the PFC chooses between conflicting options—Coke or Pepsi; blurting out what you really think or restraining yourself; pulling the trigger or not. And often the conflict being resolved is between a decision heavily driven by cognition and one driven by emotions. Once it has decided, the PFC sends orders via projections to the rest of the frontal cortex, sitting just behind it. Those neurons then talk to the “premotor cortex,” sitting just behind it, which then passes it to the “motor cortex,” which talks to your muscles. And a behavior ensues.*  Before considering how the frontal cortex influences social behavior, let’s start with a simpler domain of its function. The Frontal Cortex and Cognition What does “doing the harder thing when it’s the right thing to do” look like in the realm of cognition (defined by Princeton’s Jonathan Cohen as “the ability to orchestrate thought and action in accordance with internal goals”)?38 Suppose you’ve looked up a phone number in a city where you once lived. The frontal cortex not only remembers it long enough to dial but also considers it strategically. Just before dialing, you consciously recall that it is in that other city and retrieve your memory of the city’s area code. And then you remember to dial “1” before the area code.* The frontal cortex is also concerned with focusing on a task. If you step off the curb planning to jaywalk, you look at traffic, paying attention to motion, calculating whether you can cross safely. If you step off looking for a taxi, you pay attention to whether a car has one of those lit taxicab thingies on top. In a great study, monkeys were trained to look at a screen of dots of various colors moving in particular directions; depending on a signal, a monkey had to pay attention to either color or movement. Each signal indicating a shift in tasks triggered a burst of PFC activity and, coupled with that, suppression of the stream of information (color or movement) that was now irrelevant. This is the PFC getting you to do the harder thing; remembering that the rule has changed, don’t do the previous habitual response.39 The frontal cortex also mediates “executive function”—considering bits of information, looking for patterns, and then choosing a strategic action.40 Consider this truly frontally demanding test. The experimenter tells a masochistic volunteer, “I’m going to the market and I’m going to buy peaches, cornflakes, laundry detergent, cinnamon...” Sixteen items recited, the volunteer is asked to repeat the list. Maybe they correctly recall the first few, the last few, list some near misses—say, nutmeg instead of cinnamon. Then the experimenter repeats the same list. This time the volunteer remembers a few more, avoids repeating the nutmeg incident. Now do it again and again. This is more than a simple memory test. With repetition, subjects notice that four of the items are fruits, four for cleaning, four spices, four carbs. They come in categories. And this changes subjects’ encoding strategy as they start clumping by semantic group—“Peaches. Apples. Blueberries—no, I mean blackberries. There was another fruit, can’t remember what. Okay, cornflakes, bread, doughnuts, muffins. Cumin, nutmeg—argh, again!—I mean cinnamon, oregano...” And throughout, the PFC imposes an overarching executive strategy for remembering these sixteen factoids.* The PFC is essential for categorical thinking, for organizing and thinking about bits of information with different labels. The PFC groups apples and peaches as closer to each other in a conceptual map than are apples and toilet plungers. In a relevant study, monkeys were trained to differentiate between pictures of a dog and of a cat. The PFC contained individual neurons that responded to “dog” and others that responded to “cat.” Now the scientists morphed the pictures together, creating hybrids with varying percentages of dog and cat. “Dog” PFC neurons responded about as much to hybrids that were 80 percent dog and 20 percent cat, or 60:40, as to 100 percent dog. But not to 40:60 —“cat” neurons would kick in there.41 The frontal cortex aids the underdog outcome, fueled by thoughts supplied from influences that fill the rest of this book—stop, those aren’t your cookies; you’ll go to hell; self-discipline is good; you’re happier when you’re thinner— all giving some lone inhibitory motor neuron more of a fighting chance. Frontal Metabolism and an Implicit Vulnerability This raises an important point, pertinent to the social as well as cognitive functions of the frontal cortex.42 All this “I wouldn’t do that if I were you”–ing by the frontal cortex is taxing. Other brain regions respond to instances of some contingency; the frontal cortex tracks rules. Just think how around age three, our frontal cortices learned a rule followed for the rest of our lives—don’t pee whenever you feel like it—and gained the means to enact that rule by increasing their influence over neurons regulating the bladder. Moreover, the frontal mantra of “self-discipline is good” when cookies beckon is also invoked when economizing to increase retirement savings. Frontal cortical neurons are generalists, with broad patterns of projections, which makes for more work.43 All this takes energy, and when it is working hard, the frontal cortex has an extremely high metabolic rate and rates of activation of genes related to energy production.44 Willpower is more than just a metaphor; self-control is a finite resource. Frontal neurons are expensive cells, and expensive cells are vulnerable cells. Consistent with that, the frontal cortex is atypically vulnerable to various neurological insults. Pertinent to this is the concept of “cognitive load.” Make the frontal cortex work hard—a tough working-memory task, regulating social behavior, or making numerous decisions while shopping. Immediately afterward performance on a different frontally dependent task declines.45 Likewise during multitasking, where PFC neurons simultaneously participate in multiple activated circuits. Importantly, increase cognitive load on the frontal cortex, and afterward subjects become less prosocial*—less charitable or helpful, more likely to lie.46 Or increase cognitive load with a task requiring difficult emotional regulation, and subjects cheat more on their diets afterward.*47 So the frontal cortex is awash in Calvinist self-discipline, a superego with its nose to the grindstone.48 But as an important qualifier, soon after we’re potty- trained, doing the harder thing with our bladder muscles becomes automatic. Likewise with other initially demanding frontal tasks. For example, you’re learning a piece of music on the piano, there’s a difficult trill, and each time as you approach it, you think, “Here it comes. Remember, tuck my elbow in, lead with my thumb.” A classic working-memory task. And then one day you realize that you’re five measures past the trill, it went fine, and you didn’t have to think about it. And that’s when doing the trill is transferred from the frontal cortex to more reflexive brain regions (e.g., the cerebellum). This transition to automaticity also happens when you get good at a sport, when metaphorically your body knows what to do without your thinking about it. The chapter on morality considers automaticity in a more important realm. Is resisting lying a demanding task for your frontal cortex, or is it effortless habit? As we’ll see, honesty often comes more easily thanks to automaticity. This helps explain the answer typically given after someone has been profoundly brave. “What were you thinking when you dove into the river to save that drowning child?” “I wasn’t thinking—before I knew it, I had jumped in.” Often the neurobiology of automaticity mediates doing the hardest moral acts, while the neurobiology of the frontal cortex mediates working hard on a term paper about the subject. The Frontal Cortex and Social Behavior  Things get interesting when the frontal cortex has to add social factors to a cognitive mix. For example, one part of the monkey PFC contains neurons that activate when the monkey makes a mistake on a cognitive task or observes another monkey doing so; some activate only when it’s a particular animal who made the mistake. In a neuroimaging study humans had to choose something, balancing feedback obtained from their own prior choices with advice from another person. Different PFC circuits tracked “reward-driven” and “advice- driven” cogitating.49 Findings like these segue into the central role of the frontal cortex in social behavior.50 This is appreciated when comparing various primates. Across primate species, the bigger the size of the average social group, the larger the relative size of the frontal cortex. This is particularly so with “fission-fusion” species, where there are times when subgroups split up and function independently for a while before regrouping. Such a social structure is demanding, requiring the scaling of appropriate behavior to subgroup size and composition. Logically, primates from fission-fusion species (chimps, bonobos, orangutans, spider monkeys) have better frontocortical inhibitory control over behavior than do non-fission-fusion primates (gorillas, capuchins, macaques). Among humans, the larger someone’s social network (measured by number of different people texted), the larger a particular PFC subregion (stay tuned).51 That’s cool, but we can’t tell if the big brain region causes the sociality or the reverse (assuming there’s causality). Another study resolves this; if rhesus monkeys are randomly placed into social groups, over the subsequent fifteen months, the bigger the group, the larger the PFC becomes—