ROBERT M SAPOLSKY “Developmental and Personal ry Correlates of Adrenocortical Activity as Indexed by Salivary Cortisol: Observations in the Age Range of 35 c0 65 Years” Journal of Psycbasomatic Raearch 35 (1991): 173. This isthe study of Hellhammer and colleagues. L. Brown, A. Tomarken, D. Orch, P Loosen, N. Kalin, and R, Davide son, "Individual Differences in Repressive-Defensiveness Predict Basal Salivary Corcsol Level.” Jourwal af Personality and Sucial Pecholopy 70 (1996): 362. R. Shaw, F. Cohen, R.Fishrran-Rosen, M. Murphy, . Scerzer, D. Cll, and K. Myler, "Psychologie Predictors of Psychosocial and Medical Outcomes in Patients Undergoing Coronary Angioplasty,” Prychaomaric Medicine 48 (1986): 582. R. Shaw; F. Cohen, B. Doyle, and J Palesky, “The Impact of Denial and Repressive Style on Information Gain and Rchabilitacion Outcomes in ‘Myocardial Infarction Patients,” Prchasmatic Medicine 47 (1985): 262. ‘A. Tomarken and R. Davidkon, “Frontal Brain Activation in Repressors and Nonrepressors,” Journal of Abnormal Payebulegy 103 (1994): 339, D. Weinberger, G. Schwara, and R. Davidson, *“Low-Anxious, High Anxious, and Repressive Coping Styles: Psychometric Patterns and Behav- ‘ral and Physiological Responses co Sttes,” Journal of Abnormal Prychology 88 (1979): 369, ‘The studies of James Gross concerning the intentional inhibition of ‘emotional expression can be found in J. Gross and R. Levenson, tional Suppression: Physiology, SelReport, and Expressive Behavior,” Jonrnal of Pronalty and Social Prychaogy 64 (1993): 870. See aso: J. Gross ‘and R. Levenson, "Hiding Feelings: The Acute Effects of Inhibiting Neg- ative and Positive Emotion," Journal of Abnormal Payholey (in ptes) 146 The Trouble with Testosterone Wilt. Boys JusT BE Boys? 6809 le Eu, Heath Thnogh Sport Th Man Cation, Howton “7about certain minorities, The stereotypes are typically pejorative and usually false. But every now and then, they are true, I writ F« it, we all do ic. Weall believe in certain stereotypes c apologeticelly as a member of a minority about which the stereotypes are indeed true. I am male, We ‘males accoune for less than 50 percent of the population, yee we generate an incredibly disproportionate percentage of the vio- lence. Whether ic is something as primal as having an ax fight in an Amazonian clearing or as detached as using computer- guided aircraft co strafe a village, someching as condemned as assauleing a cripple or as glorified as killing someone wearing the ‘wrong uniform, ifit is violene, males excel atic. Why should thac be? We all chink we know the answer. A dozen millennia ago or so, an adventurous soul managed to lop off a surly bull's testicles and thus invented behavioral endocrinology. It is unclear from the historical records whether this individual received either a grant or tenure as a result of this experiment, bur ir certainly generated an influ ‘ential finding—something or other comes out of the testes that helps co make males such aggressive pains in the ass. That something or other is testosterone.” The hormone “Testosterone is one ofa family of related hormones, collectively known, 1s “androgens” or “anabolic steroids” They all are sereted from the estes 449,ROBERT M. SAPOLSKY binds to specialized receptors in muscles and causes those cells, to enlarge. It binds to similar receptors in laryngeal cells and zives rise co operatic basses. It causes other secondary sexual characteristics, makes for relatively unhealthy blood vessels, alters biochemical events in the liver too dizzying co even con- template, has @ profound impact, no doubsr, on the workings of cells in big toes. And it seeps into the brain, where it binds to those same “androgen” receptors and influences behavior in way highly relevant co understanding aggression. ‘What evidence links testosterone with aggression? Some pretty obvious stuff: Males zend to have higher testosterone levels in their circulation than do females (one wild exception to chat will be discussed later) and eo be more aggressive. Times of life when males ace swimming in escosterone (for example, after reaching puberty) correspond co when aggres- sion peaks. Among numerous species, cesces are mothballed most of the year, kicking into action and pouring out testos- terone only during a very circumscribed mating season—pre- cisely the time when male-male aggeession soars. Impressive, but these are only correlative data, eestosterone repeatedly being on the scene with no alibi when some aggression has occurred. The proof comes with the knife, the performance of what is euphemistically known as a "subtrac- tion” experiment. Remove the source of testosterone in species after species and levels of aggression typically plum- met. Reinstare normal testosterone levels afterward with injections of synthetic testosterone, and aggression recurns. To an endocrinologist, the subtraction and replacement for are the resule of a modification of testosterone, they all have a similar chemical structure, and they all do roughly similar things. Nonetheless, androgen mavens spend entire carers seudying the important differences in the actions of differen androgens. Lam going to throw that subtlety ro the wind and, for the sake of siplification chae will hortiy many, will refer throughout to all ofthese related hormones as “ceststeron 150. : | 1 / : | | i | | ' THE TROUBLE WITH TESTOSTERONE paradigm represents preety damaing. proof: this hormone is involved. “Normal testosterone levels appear to be a prerequi- site for notmative levels of aggressive behavior” is the sore of catchy, hummable phrase that the eextbooks would use. ‘That probably explains why you shouldn't mess wich a bull moose duting rutting season. But that’s not why a lot of people wane to understand this sliver of scierce. Does the action of this hormone tell us anything about individual differences in levels of aggression, anything about why some males, some human, males, are exceptionally violenc? Among. an array of males— human or otherwise—are the highest eestosterone levels found in the most aggressive individuals? Generate some extreme differences and that is precisely what you see. Castrate some of che well-paid seudy subjects, inject others with enough testosterone to quadruple the normal human levels, and che high-testosterone males are over- whelmingly likely to be the more aggressive ones. However, that loesn't tell us much about the real world. Now do something, more subtle by studying the normative vaciabilicy ia cestos- tetone—in other words, don’t manipulate anything, just see what everyone's natural levels are like—and high levels of testosterone and high levels of aggression still cend co go together. This would seem eo seal che case—interindividual dif ferences in levels of aggression among normal individuals are probably driven by differences in levels of testosterone. But this, turns out to be wrong. Okay, suppose you note a co:relation becween levels of aggression and levels of testosterone among these normal ‘males. This could be because (a) testosterone elevates aggres- sion; (L) aggression elevates testosterone secretion; (c) neither causes the other. There's a huge bias to assume option 4, while ‘is the answer. Study after scudy has shown that when you examine testosterone levels when males are first placed cogether in the social group, testosterone levels predice noth 151 : a3 so FensROBERT M, SAPOLSKY ing about who is going to be aggressive. The subsequent behavioral differences drive che hormonal changes, racher than the other way around. Because of a strong bias among certain scientists, it has taken forever co convince them of this point. Behavioral cendocrinologists study what behavior and hormones have to do ‘with each other. How do you study behavior? You get yourself a notebook and a stopwatch and a pair of binoculars. How do you measure the hormones? You need a gazillion-dollar machine, you muck around with radiation and chemicals, wear a lab coat, maybe even goggles—the whole nine yards. Which coys would you ra:her get for Christmas? Which facet of science are you going to believe in more? Because che endocrine aspects of the business are more high-tech, more reductive, there is the bias to think thae it is somehow more scientific, more powerful. This is a classic case of what is often called physics envy, the disease among scientists where the behavioral biologists fear their discipline lacks the rigor of physiology, the physiologists wish for the techniques of the bio- chemists, the biochemists covet the clarity of che answers revealed by the molecula” biologists, all the way down until you get co the physicists, who confer only with God.” Hor- ‘mones seem to many co be more real, more substantive, chan the ephemera of behavier, so when a correlation occurs, it “An example of physics ervy in action. Recently, a zoologist friend had obtained blood samples from the carnivores thae he studies and syanted some hormones in thesample assays in my lab, Alehough inexpe= rienced with the technique, he olfered to help in any way possible. I ele hesicant asking him co do anything cedious bat, so long as he had offered, reneativly sad, “Well if you don’e mind some unspeakable drudgery, you ‘ould number aboue a chousand assay vials.” And chis scientist, whose superb work has graced the mest prestigious science journals in the world, cheerfully answered, "Thar's ay, how often do I get to do rea! science, working with tse cubes?” THE TROUBLE WITH TESTOSTERONE must be because hormones regulate behavior, not che ocher way around. As I said, ie eakes a lot of work to cure people of chat physics envy, and to see that interindividual differences in testosterone levels don’e predict subsequent differences in aggressive behavior among individuals. Similarly, fluctuations in cescosterone levels within one individual over time do not predict subsequent changes in the levels of aggression in that one individual—gee a hiccup in testosterone secretion one afternoon and that's not when the guy goes postal Look at our confusing state: normal levels of testosterone are a prerequisite for normal levels of aggression, yet chang- ing the amoune of testosterone in someone's bloodscream within the normal range doesn't alter his subsequent levels of aggressive behavior. This is where, like clockwork, the stu- dents suddenly stare coming ec office hours in a panic, asking, whether they missed something in their leccure notes. s going to be on the final, and it’s one of the more subtle points in endocrinology—whar is referred to as a hor- mone having a “permissive effect.” Remove someone's testes and, as noted, the frequency of aggressive behavior is likely to plummet. Reinseate precastration levels of testosterone by injecting that hormone, and precastration levels of aggression typically return. Fair enough. Now this time, castrate an indi- vidual and rescore testosterone levels to only 20 percent of normal and. . . amazingly, normal precastration levels of aggression come back. Castrate and now generate twice che cestosterone levels from before castration—and the same level of aggressive behavior returns. You need some testosterone around for normal aggressive behavior—zero levels after cas- tration, and down it usually goes; quadruple it (che sore of range generated in weighe lifters abusing anabolic steroids), and aggression typically increases. Buc anywhere from roughly 20 percent of normal co twice normal and it's all theROBERT M SAPOLSKY same; the brain can’t distinguish among this wide range of basically normal values. ‘We seem to have figured out a couple of things by now. First, knowing the differences in che levels of eestosterone in the cir- culation of a bunch of males will nor help you much in figue- ing out who is going to be aggressive. Second, the subtraction and reinstarement data seem to indicate that, nevertheless, in a broad sort of way, testosterone causes aggressive behavior. But chae euens out not cobe erue either, and the implications of this are lost on most peosle the first thirty times you tell chem about it. Which is why you'd better cell them abouc ie thirty- cone times, because it is tae most important point ofthis piece. Round up some male monkeys. Put them in a group cogether, and give them plenty of time to sore oue where they stand wich each other—affiliative fiiendships, grudges and dislikes. Give them enough time to form a dominance hierarchy, a linear rank- ing system of numbers I through 5. This is the hierarchical sore of system where number 3, for example, can pass his day throwing around his weight with numbers 4 and 5, ripping off their monkey chow, forcing them co relinquish the best spots ¢o sie in, but, atthe same time, remembering to deal with num- bers 1 and 2 with shit-eating obsequiousness. Hierarchy in place, it’s time to do your experiment. ‘Take thac third-ranking monkey and give him some testosterone. None of this within-the-normal-range stuff. Inject a ton of it into him, way higher ehan what you normally see in a rhesus monkey; give him enough testosterone to grow antlers and a beard on every ncuron in his brain. And, no surprise, when you then check the behavioral data, it curns oue that he will probably be participating in more aguressive interactions than before. So even though small fluctuations in che levels of the hor- mone don't seem to matter much, testosterone still causes THE ROUBLE WITH TESTOSTERONE aggression. Bue chat would be wrong. Check out number 3 more closely. Is he now raining aggressive terror on any and all in the group, frothing in an androgenic glaze of indiscriminate violence? Not at all. He's still jdiciously koweowing co num- bers 1 and 2, but has simply become a total bastard to num- bers 4 and 5. This is critical: testosterone isn’t causing aggression, it's exaggenting che aggression that's alzeady there. ‘Another example just co show we're serious. There's a part of your brain thae probably has lots to do with aggression, a region called che amygdala.” Sitting righe near ic is che Grand ‘Central Seation of emotion-related activity in your brain, the hypothalamus. The amygdala communicates wich the hypo- thalamus by way of a cable of neuro: stria terminalis, No more jargon, I promise. The amygdala has its influence on aggression via that pathway, wich bursts of electrical excication called action potentials thac ripple down the stria terminalis, putcing the hypothalamus in a pissy mood. ‘Once again, do your hormonal intervention; flood the area with cestosterone. You can do that by injecting che hormone into the bloodstream, where it eventually makes its way t0 this part of the brain. Or you can be elegant and surgically icroinjece the stuff directly into this brain region. Six of one, half-a dozen of the other. The key thing is what doesn’t hap- pen next. Does testosterone now cause there to be action potentials surging down the seria terminalis? Does it turn on. hae pathway? Not at all. Ifand only if the amygdala is ready sending an aggression-provoking volley of action potentials down the stria terminalis, testosterone increases the rate of Ul connections called the such action potentials by shortening the resting cine between “And no one has shown thae differences in che size or shape of the amygdala, or eliferences in the numbers of neurons in i, can begin co p dice differences in normal levels of aggression. Same punch line as wichROBERT M SAPOLSKY chem, It's not curning on the pathway, it's increasing che vol- ume of signaling if it is already curned on. Ie's not causing aggression, it’s exaggerating the preexisting pattern of it, exaggerating che response co environmental criggers of aggression. This cranscends issues of testosterone and aggression. In every generation, ic is the duty of behavioral biologists to uy to teach this critical point, one that seems a maddening clic once you get it. You take thac hoary old dichotomy between nature and nurture, between biological influences and envi- ronmencal influences, between intrinsic factors and extrinsic ones, and, che vast majority of the time, regardless of which behavior you are thinking about and what underlying biology you are studying, the dichotomy is a sham. No biology. No environment. Just the interaction between the ewo. Do you want to know how important environment and experience are in understanding testosterone and aggression? Look back at how che effects of castration were discussed ear- lier. There were statements like “Remove the source of testos- terone in species after species and levels of aggression typically plummer.” Nor “Remove the source . .. and aggression always goes co zero.” On the average it declines, but rarely co zero, and not at all in some individuals, And the more social experience an individual hid being aggressive prior to castra- tion, the more likely chat Sehavior persists sans wnjones. Social conditioning can more than make up for the hormone. Another example, one from one of the stranger comers of the animal kingdom: If yo1 want your assumptions about the nacure of boy beasts and girl beasts challenged, check out the spotted hyena. These animals are fast becoming the dar- lings of endocrinologists, sociobiologists, gynecologists, and tabloid writers. Why? Because they have a wild sex-reversal system—females are more muscular and more aggressive than males and are socially dominant over them, rare traits in 156 THE TROUBLE WITH TESTOSTERONE, the mammalian world. And get this: females secrete more of ‘certain cestosterone-relaced hormones than the males do, pro- ducing the muscles, che aggression (and, as a reason for much of the gawking interese in these animals, wildly masculinized private parts that make it supremely difficule eo tell the sex of a hyena), So chis appears to bea strong vote for the causative powers of high ancliogen levels in aggression and social domi- nance. Bue that's not the whole answer. High up in che above the University of California at Berkeley is the world’s largest colony of spotted hyenas, massive bone-crunching beasts who fight with each other for che chance to have their cars scratched by Laurence Frank, che zoologist who brought, them over as infants from Kenya. Various scientists are seudy- ing their sex-reversal system. The female hyenas are bigger and more muscular than the males and have the same weirdo genitals and elevated androgen levels chat their female cousins do back in the savannah. Everything is in place except the social system is completely different from chat in che wild. Despiee being stoked on androgens, there is a very sig- nificant delay in the time it takes for the females to begin socially dominating the males—they’re growing up without the established social system to learn from When people first grasp the extent to which biology has something to do wich behavior, even subtle, complex, human behavior, there is often an initial evangelical enthusiasm of the convert, a massive placing of faith in che biological compo- nents of the story. And this enthusiasm is typically of a fairly reductive type—because of physics envy, because reduction- ism is so impressive, because it would be so nice if there were a single gene ot hormone or neurotransmitcer or part of the brain chat was it, che cause, the explanation of everything. And the trouble with testosterone is that people tend to think. this way in an arena chat really matters. ‘This is no mere academic concern, We are a fine species 157ROBERT M. SAPOLSKY with some potential. Yee we are racked by sickening amounts of violence. Unless we are hermies, we feel the threat of it, often as a daily shadow. And regardless of where we hide, should our leaders push the bueton, we will all be lose in a final global violence. Buc as we try to understand and wrestle with this feature of our sociality, i i critical co remember the limits of the biology. Testcsterone ie never going co tell us much about the suburban teenager who, in his after-school cchess club, has developed a particularly aggressive style with his bishops. And ie certainly isn’e going co cell us much about the teenager in some inner-city hellhole who has taken to mugging people. “Testosterone equals aggression” is inade- quate for those who would offer a simple solution to the vio- lent male—just decrease levels of chose pesky steroids. And “testosterone equals aggression” is certainly inadequate for those who would offer a simple excuse: Boys will be boys and certain things in nature are inevitable. Violence is more com- plex than a single hormone. This is endocrinology for the bleeding heart liberal—ovr behavioral biology is usually meaningless outside the context of the social faccors and envi- ronmenc in which ie occurs. FURTHER READING Fora good general review ofthe subject, sce B. Monaghan and S. Glick ‘man, “Hormones and Aggressive Behavior” in J. Becker, M. Breedlove, and D. Crews, eds., Behavional Endocrinology (Cambridge, Mass.: MIT Press, 1992), 261. This also has sa overview of the hyena social syscem, as Glickman heads the study of the Berkeley hyenas. For eeclnical papers on the acquisition of the female dominance in hyenas, see $. Jenks, M. Weldele, L Frank, and S. Glickman, “Acquisition of Macrilineal Rank in ‘Captive Spotted Hyenas: Emergence of a Natural Social System i Pece- Reared Animals and Theie Offspring," Animal Belvier 50 (1995): 8935 and L. Frank, S. Glickman, and C. Zabel, “Oneogeny of Female Domi 158, THE TROUBLE WITH TESTOSTERONE nance in the Spotted Hyaena: Perspectives from Nature and Captivity” in P Jewell and G, Maloy, eds., “The Biology of Large African Mammals in ‘Theie Environment,” Syuporium ofthe Zeobgicl Society of London 61 (1989) 127. have emphasized thae while testosterone levels in che normal range do fot have much to do with aggression, a massive elevation of exposure, as would be seen in anabolic steroid abusers, does usually increase aggression. For a tecent seuly in which even clovacng into char range (approximately five times normal level) still had no eect on mood or behavior, see S. Bhasin, T. Scorer, N, Berman, and celleagues, “The Effects of Supra- physiologic Doses of Testosterone on Muscle Size and Strengeh in Normal Men,” New England Jauraa of Medicine 335 (1996): “The study showing chat raising testosterone levels in che middle- ranking monkey exaggerates preexisting patterns of aggression can be found in A. Dixson and J. Hesbert, "Testosterone, Aggressive Behavior and Dominance Rank in Captive Adule Male Talapoin Monkeys (Mfopithe- «us talapin)," Physiology and Bebaaior 18 (1977: 539. For the demonstra~ tion thac testosterone shorcens the cesting period between action potentials in neurons, sce K. Kendrick and R, Drewett, “Testosterone [Reduces Refractory Period of Seria Terminalis Neutons in the Rat Brain,” Seinas 204 (1979): 877, 159