Behave: The Biology of Humans at Our Best and Worst

by Robert M. Sapolsky

  32.C. Heim et al., “Pituitary-Adrenal and Autonomic Responses to Stress in Women After Sexual and Physical Abuse in Childhood,” JAMA 284 (2000): 592; E. Binder et al., “Association of FKBP5 Polymorphisms and Childhood Abuse with Risk of Posttraumatic Stress Disorder Symptoms in Adults,” JAMA 299 (2008): 1291; C. Heim et al., “The Dexamethasone/Corticotropin-Releasing Factor Test in Men with Major Depression: Role of Childhood Trauma,” BP 63 (2008): 398; R. Lee et al., “Childhood Trauma and Personality Disorder: Positive Correlation with Adult CSF Corticotropin-Releasing Factor Concentrations,” Am J Psychiatry 162 (2005): 995; R. J. Lee et al., “CSF Corticotropin-Releasing Factor in Personality Disorder: Relationship with Self-Reported Parental Care,” Neuropsychopharmacology 31: (2006): 2289; L. Carpenter et al., “Cerebrospinal Fluid Corticotropin-Releasing Factor and Perceived Early-Life Stress in Depressed Patients and Healthy Control Subjects,” Neuropsychopharmacology 29 (2004): 777; T. Rinne et al., “Hyperresponsiveness of Hypothalamic-Pituitary-Adrenal Axis to Combined Dexamethasone/Corticotropin-Releasing Hormone Challenge in Female Borderline Personality Disorder Subjects with a History of Sustained Childhood Abuse,” BP 52 (2002): 1102; P. McGowan et al., “Epigenetic Regulation of the Glucocorticoid Receptor in Human Brain Associates with Childhood Abuse,” Nat Nsci 12 (2009): 342; M. Toth et al., “Post-weaning Social Isolation Induces Abnormal Forms of Aggression in Conjunction with Increased Glucocorticoid and Autonomic Stress Responses,” Horm Behav 60 (2011): 28.

  33.S. Lupien et al., “Effects of Stress Throughout the Lifespan on the Brain, Behaviour and Cognition,” Nat Rev Nsci 10 (2009): 434; V. Carrion et al., “Stress Predicts Brain Changes in Children: A Pilot Longitudinal Study on Youth Stress, Posttraumatic Stress Disorder, and the Hippocampus,” Pediatrics 119 (2007): 509; F. L. Woon and D. W. Hedges, “Hippocampal and Amygdala Volumes in Children and Adults with Childhood Maltreatment–Related Posttraumatic Stress Disorder: A Meta-analysis,” Hippocampus 18 (2008): 729.

  34.S. J. Lupien et al., “Effects of Stress Throughout the Lifespan on the Brain, Behaviour and Cognition,” Nat Rev Nsci 10 (2009): 434; D. Hackman et al., “Socioeconomic Status and the Brain: Mechanistic Insights from Human and Animal Research,” Nat Rev Nsci 11 (2010): 651; M. Sheridan et al., “The Impact of Social Disparity on Prefrontal Function in Childhood,” PLoS ONE 7 (2012): e35744; J. L. Hanson et al., “Structural Variations in Prefrontal Cortex Mediate the Relationship Between Early Childhood Stress and Spatial Working Memory,” J Nsci 32 (2012): 7917; M. Sweitzer et al., “Polymorphic Variation in the Dopamine D4 Receptor Predicts Delay Discounting as a Function of Childhood Socioeconomic Status: Evidence for Differential Susceptibility,” SCAN 8 (2013): 499; E. Tucker-Drob et al., “Emergence of a Gene X Socioeconomic Status Interaction on Infant Mental Ability Between 10 Months and 2 Years,” Psych Sci 22 (2011): 125; I. Liberzon et al., “Childhood Poverty Alters Emotional Regulation in Adulthood,” SCAN 10 (2015): 1596; K. G. Noble et al., “Family Income, Parental Education and Brain Structure in Children and Adolescents,” Nat Nsci 18 (2015): 773.

  35.Footnote: R. Nevin, “Understanding International Crime Trends: The Legacy of Preschool Lead Exposure,” Environmental Res 104 (2007): 315.

  36.Reviewed in R. Sapolsky, Why Zebras Don’t Get Ulcers: A Guide to Stress, Stress-Related Diseases and Coping, 3rd ed. (New York: Holt, 2004). Baboon equivalent: P. O. Onyango et al., “Persistence of Maternal Effects in Baboons: Mother’s Dominance Rank at Son’s Conception Predicts Stress Hormone Levels in Subadult Males,” Horm Behav 54 (2008): 319.

  37.F. L. Woon and D. W. Hedges, “Hippocampal and Amygdala Volumes in Children and Adults with Childhood Maltreatment–Related Posttraumatic Stress Disorder: A Meta-analysis,” Hippocampus 18 (2008): 729; D. Gee et al., “Early Developmental Emergence of Human Amygdala-PFC Connectivity After Maternal Deprivation,” PNAS 110 (2013): 15638; A. K. Olsavsky et al., “Indiscriminate Amygdala Response to Mothers and Strangers After Early Maternal Deprivation,” BP 74 (2013): 853.

  38.L. M. Oswald et al., “History of Childhood Adversity Is Positively Associated with Ventral Striatal Dopamine Responses to Amphetamine,” Psychopharmacology (Berlin) 23 (2014): 2417; E. Hensleigh and L. M. Pritchard, “Maternal Separation Increases Methamphetamine-Induced Damage in the Striatum in Male, But Not Female Rats,” BBS 295 (2014): 3; A. N. Karkhanis et al., “Social Isolation Rearing Increases Nucleus Accumbens Dopamine and Norepinephrine Responses to Acute Ethanol in Adulthood,” Alcohol: Clin Exp Res 38 (2014): 2770.

  39.C. Anacker et al., “Early Life Adversity and the Epigenetic Programming of Hypothalamic-Pituitary-Adrenal Function,” Dialogues in Clin Nsci 16 (2014): 321.

  40.S. L. Buka et al., “Youth Exposure to Violence: Prevalence, Risks, and Consequences,” Am J Orthopsychiatry 71 (2001): 298; M. B. Selner-O’Hagan et al., “Assessing Exposure to Violence in Urban Youth,” J Child Psych and Psychiatry 39 (1998): 215; P. T. Sharkey et al., “The Effect of Local Violence on Children’s Attention and Impulse Control,” Am J Public Health 102 (2012): 2287; J. B. Bingenheimer et al., “Firearm Violence Exposure and Serious Violent Behavior,” Sci 308 (2005): 1323. Footnote: I. Shaley et al., “Exposure to Violence During Childhood Is Associated with Telomere Erosion from 5 to 10 Years of Age: A Longitudinal Study,” Mol Psychiatry 18 (2013): 576.

  41.For a particularly good review, see L. Huesmann and L. Taylor, “The Role of Media Violence in Violent Behavior,” Ann Rev of Public Health 27 (2006): 393. See also J. D. Johnson et al., “Differential Gender Effects of Exposure to Rap Music on African American Adolescents’ Acceptance of Teen Dating Violence,” Sex Roles 33 (1995): 597; J. Johnson et al., “Television Viewing and Aggressive Behavior During Adolescence and Adulthood,” Sci 295 (2002): 2468; J. Savage and C. Yancey, “The Effects of Media Violence Exposure on Criminal Aggression: A Meta-analysis,” Criminal Justice and Behav 35 (2008): 772; C. Anderson et al., “Violent Video Game Effects on Aggression, Empathy, and Prosocial Behavior in Eastern and Western Countries: A Meta-analytic Review,” Psych Bull 136, 151; C. J. Ferguson, “Evidence for Publication Bias in Video Game Violence Effects Literature: A Meta-analytic Review,” Aggression and Violent Behavior 12 (2007): 470; C. Ferguson, “The Good, the Bad and the Ugly: A Meta-analytic Review of Positive and Negative Effects of Violent Video Games,” Psychiatric Quarterly 78 (2007): 309.

  42.W. Copeland et al., “Adult Psychiatric Outcomes of Bullying and Being Bullied by Peers in Childhood and Adolescence,” JAMA Psychiatry 70 (2013): 419; S. Woods and E. White, “The Association Between Bullying Behaviour, Arousal Levels and Behaviour Problems,” J Adolescence 28 (2005): 381; D. Jolliffe and D. P. Farrington, “Examining the Relationship Between Low Empathy and Bullying,” Aggressive Behav 32 (2006): 540; G. Gini, “Social Cognition and Moral Cognition in Bullying: What’s Wrong?” Aggressive Behav 32 (2006): 528; S. Shakoor et al., “A Prospective Longitudinal Study of Children’s Theory of Mind and Adolescent Involvement in Bullying,” J Child Psych and Psychiatry 53 (2012): 254.

  43.J. D. Unenever, “Bullies, Aggressive Victims, and Victims: Are They Distinct Groups?” Aggressive Behav 31 (2005): 153; D. P. Farrington and M. M. Tofi, “Bullying as a Predictor of Offending, Violence and Later Life Outcomes,” Criminal Behaviour and Mental Health 21 (2011): 90; M. Tofi et al., “The Predictive Efficiency of School Bullying Versus Later Offending: A Systematic/Meta-analytic Review of Longitudinal Studies,” Criminal Behaviour and Mental Health 21 (2011): 80; T. R. Nansel et al., “Cross-National Consistency in the Relationship Between Bullying Behaviors and Psychosocial Adjustment,” Arch Pediatrics & Adolescent Med 158 (2004): 730; J. A. Stein et al., “Adolescent Male Bullies, Victims, and Bully-Victims: A Comparison of Psychosocial and Behavioral Characteristics,” J Pediatric Psych 32 (2007): 273; P. W. Jansen et al., “Prevalence of Bullying and Victimization Among Children in Early Elementary School: Do Family and School Neighbourhood Socioeconomic Status Matter?” BMC Public Health 12 (2012): 494; A. Sourander et al., �
�What Is the Early Adulthood Outcome of Boys Who Bully or Are Bullied in Childhood? The Finnish ‘From a Boy to a Man’ Study,” Pediatrics 120 (August 2007): 397; A. Sourander et al., “Childhood Bullies and Victims and Their Risk of Criminality in Late Adolescence,” Arch Pediatrics & Adolescent Med 161 (2007): 546; C. Winsper et al., “Involvement in Bullying and Suicide-Related Behavior at 11 Years: A Prospective Birth Cohort Study,” J the Am Academy of Child and Adolescent Psychiatry 51 (2012): 271; F. Elgar et al., “Income Inequality and School Bullying: Multilevel Study of Adolescents in 37 Countries,” J Adolescent Health 45 (2009): 351.

  44.G. M. Glew et al., “Bullying, Psychosocial Adjustment, and Academic Performance in Elementary School,” Arch Pediatrics & Adolescent Med 159 (2005): 1026.

  45.K. Appleyard et al., “When More Is Not Better: The Role of Cumulative Risk in Child Behavior Outcomes,” J Child Psych and Psychiatry 46 (2005): 235.

  46.M. Sheridan et al., “Variation in Neural Development as a Result of Exposure to Institutionalization Early in Childhood,” PNAS 109 (2012): 12927; M. Carlson and F. Earis, “Psychological and Neuroendocrinological Sequelae of Early Social Deprivation in Institutionalized Children in Romania,” ANYAS 15 (1997): 419; N. Tottenham, “Human Amygdala Development in the Absence of Species-Expected Caregiving,” Developmental Psychobiology 54 (2012): 598; M. A. Mehta et al., “Amygdala, Hippocampal and Corpus Callosum Size Following Severe Early Institutional Deprivation: The English and Romanian Adoptees Study Pilot,” J Child Psych and Psychiatry 50 (2009): 943; N. Tottenham et al., “Prolonged Institutional Rearing Is Associated with Atypically Large Amygdala Volume and Difficulties in Emotion Regulation,” Developmental Sci 13 (2010): 46; M. M. Loman et al., “The Effect of Early Deprivation on Executive Attention in Middle Childhood,” J Child Psych and Psychiatry 54 (2012): 37; T. Eluvathingal et al., “Abnormal Brain Connectivity in Children After Early Severe Socioemotional Deprivation: A Diffusion Tensor Imaging Study,” Pediatrics 117 (2006): 2093; H. T. Chugani et al., “Local Brain Functional Activity Following Early Deprivation: A Study of Postinstitutionalized Romanian Orphans,” Neuroimage 14 (2001): 1290.

  47.Her idea is nicely summarized in M. Small, Our Babies, Ourselves (New York: Anchor Books, 1999).

  48.H. Arendt, The Origins of Totalitarianism (New York: Harcourt 1951); T. Adorno et al., The Authoritarian Personality (New York: Harper & Row, 1950).

  49.D. Baumrind, “Child Care Practices Anteceding Three Patterns of Preschool Behavior,” Genetic Psych Monographs 75 (1967): 43.

  50.E. E. Maccoby and J. A. Martin, “Socialization in the Context of the Family: Parent-Child Interaction,” in Handbook of Child Psychology, ed. P. Mussen (New York: Wiley, 1983).

  51.J. R. Harris, The Nurture Assumption: Why Children Turn Out the Way They Do (New York: Simon & Schuster, 1998).

  52.J. Huizinga, Homo Ludens: A Study of the Play-Element in Culture (London: Routledge & Kegan Paul, 1938); A. Berghänel et al., “Locomotor Play Drives Motor Skill Acquisition at the Expense of Growth: A Life History Trade-off,” Sci Advances 1 (2015): 1; J. Panksepp and W. W. Beatty, “Social Deprivation and Play in Rats,” Behav and Neural Biol 39 (1980): 197; M. Bekoff and J. A. Byers, Animal Play: Evolutionary, Comparative, and Ecological Perspectives (Cambridge: Cambridge University Press, 1998); M. Spinka et al., “Mammalian Play: Training for the Unexpected,” Quarterly Rev of Biol 76 (2001): 141.

  53.S. M. Pellis, “Sex Differences in Play Fighting Revisited: Traditional and Nontraditional Mechanisms of Sexual Differentiation in Rats,” Arch Sexual Behav 31 (2002): 17; B. Knutson et al., “Ultrasonic Vocalizations as Indices of Affective States in Rats,” Psych Bull 128 (2002): 961; Y. Delville et al., “Development of Aggression,” in Biology of Aggression, ed. R. Nelson (Oxford: Oxford University Press, 2005).

  54.J. Tsai, “Ideal Affect: Cultural Causes and Behavioral Consequences,” Perspectives on Psych Sci 2 (2007): 242; S. Kitayama and A. Uskul, “Culture, Mind, and the Brain: Current Evidence and Future Directions,” Ann Rev of Psych 62 (2011): 419.

  55.C. Kobayashi et al., “Cultural and Linguistic Influence on Neural Bases of ‘Theory of Mind’: An fMRI Study with Japanese Bilinguals,” Brain and Language 98 (2006): 210; C. Lewis et al., “Social Influences on False Belief Access: Specific Sibling Influences or General Apprenticeship?” Child Development 67 (1996): 2930; J. Perner et al., “Theory of Mind Is Contagious: You Catch It from Your Sibs,” Child Development 65 (1994): 1228; D. Liu et al., “Theory of Mind Development in Chinese Children: A Meta-analysis of False-Belief Understanding Across Cultures and Languages,” Developmental Psych 44 (2008): 523.

  56.C. Anderson et al., “Violent Video Game Effects on Aggression, Empathy, and Prosocial Behavior in Eastern and Western Countries: A Meta-analytic Review,” Psych Bull 136 (2010): 151.

  57.R. E. Nisbett and D. Cohen, Culture of Honor: The Psychology of Violence in the South (Boulder, CO: Westview Press, 1996).

  58.A. Kusserow, “De-homogenizing American Individualism: Socializing Hard and Soft Individualism in Manhattan and Queens,” Ethos 27 (1999): 210.

  59.S. Ullal-Gupta et al., “Linking Prenatal Experience to the Emerging Musical Mind,” Front Systems Nsci 3 (2013): 48.

  60.A. DeCasper and W. Fifer, “Of Human Bonding: Newborns Prefer Their Mothers’ Voices,” Sci 6 (1980): 208; A. J. DeCasper and P. A. Prescott, “Human Newborns’ Perception of Male Voices: Preference, Discrimination, and Reinforcing Value,” Developmental Psychobiology 17 (1984): 481; B. Mampe et al., “Newborns’ Cry Melody Is Shaped by Their Native Language,” Curr Biol 19 (2009): 1994; A. DeCasper and M. Spence, “Prenatal Maternal Speech Influences Newborns’ Perception of Speech Sounds,” Infant Behav and Development 9 (1986): 133.

  61.J. P. Lecanuet et al., “Fetal Perception and Discrimination of Speech Stimuli: Demonstration by Cardiac Reactivity: Preliminary Results,” Comptes rendus de l’Académie des sciences III 305 (1987): 161; J. P. Lecanuet et al., “Fetal Discrimination of Low-Pitched Musical Notes,” Developmental Psychobiology 36 (2000): 29; C. Granier-Deferre et al., “A Melodic Contour Repeatedly Experienced by Human Near-Term Fetuses Elicits a Profound Cardiac Reaction One Month After Birth,” PLoS ONE 23 (2011): e17304.

  62.G. Kolata, “Studying Learning in the Womb,” Sci 225 (1984): 302; A. J. DeCasper and M. J. Spence, “Prenatal Maternal Speech Influences Newborns’ Perception of Speech Sounds,” Infant Behav and Development 9 (1986): 133.

  63.P. Y. Wang et al., “Müllerian Inhibiting Substance Contributes to Sex-Linked Biases in the Brain and Behavior,” PNAS 106 (2009): 7203; S. Baron-Cohen et al., “Sex Differences in the Brain: Implications for Explaining Autism,” Sci 310 (2005): 819.

  64.R. Goy and B. McEwen, Sexual Differentiation of the Brain (Cambridge, MA: MIT Press, 1980).

  65.J. Money, “Sex Hormones and Other Variables in Human Eroticism,” in Sex and Internal Secretions, ed. W. C. Young, 3rd ed. (Baltimore: Williams and Wilkins, 1963), p. 138.

  66.G. M. Alexander and M. Hines, “Sex Differences in Response to Children’s Toys in Nonhuman Primates (Cercopithecus aethiops sabaeus),” EHB 23 (2002): 467. (This is the source of the figure in the text). J. M. Hassett et al., “Sex Differences in Rhesus Monkey Toy Preferences Parallel Those of Children,” Horm Behav 54 (2008): 359.

  67.K. Wallen and J. M. Hassett, “Sexual Differentiation of Behavior in Monkeys: Role of Prenatal Hormones,” J Neuroendocrinology 21 (2009): 421; J. Thornton et al., “Effects of Prenatal Androgens on Rhesus Monkeys: A Model System to Explore the Organizational Hypothesis in Primates,” Horm Behav 55 (2009): 633.

  68.M. Hines, Brain Gender (New York: Oxford University Press, 2004); G. A. Mathews et al., “Personality and Congenital Adrenal Hyperplasia: Possible Effects of Prenatal Androgen Exposure,” Horm Behav 55 (2009): 285; R. W. Dittmann et al., “Congenital Adrenal Hyperplasia. I: Gender-Related Behavior and Attitudes in Female Patients and Sisters,
” PNE 15 (1990): 401; A. Nordenstrom et al., “Sex-Typed Toy Play Correlates with the Degree of Prenatal Androgen Exposure Assessed by CYP21 Genotype in Girls with Congenital Adrenal Hyperplasia,” J Clin Endo and Metabolism 87 (2002): 5119; V. L. Pasterski et al., “Increased Aggression and Activity Level in 3- to 11-Year-Old Girls with Congenital Adrenal Hyperplasia,” Horm Behav 52 (2007): 368.

  69.C. A. Quigley et al., “Androgen Receptor Defects: Historical, Clinical, and Molecular Perspectives,” Endocrine Rev 16 (1995): 271; N. P. Mongan et al., “Androgen Insensitivity Syndrome,” Best Practice & Res: Clin Endo & Metabolism 29 (2015): 569.

  70.F. Brunner et al., “Body and Gender Experience in Persons with Complete Androgen Insensitivity Syndrome,” Zeitschrift für Sexualforschung 25 (2012): 26; F. Brunner et al., “Gender Role, Gender Identity and Sexual Orientation in CAIS (‘XY-Women’) Compared with Subfertile and Infertile 46,XX Women,” J Sex Res 2 (2015): 1; D. G. Zuloaga et al., “The Role of Androgen Receptors in the Masculinization of Brain and Behavior: What We’ve Learned from the Testicular Feminization Mutation,” Horm Behav 53 (2008): 613; H. F. L. Meyer-Bahlburg, “Gender Outcome in 46,XY Complete Androgen Insensitivity Syndrome: Comment on T’Sjoen et al.,” Arch Sexual Behav 39 (2010): 1221; G. T’Sjoen et al., “Male Gender Identity in Complete Androgen Insensitivity Syndrome,” Arch Sexual Behav 40 (2011): 635.

  71.J. Hönekopp et al., “2nd to 4th Digit Length Ratio (2D:4D) and Adult Sex Hormone Levels: New Data and a Meta-analytic Review,” PNE 32 (2007): 313.

  72.Findings from males regarding aggression and assertiveness: C. Joyce et al., “2nd to 4th Digit Ratio Confirms Aggressive Tendencies in Patients with Boxers Fractures,” Injury 44 (2013): 1636; M. Butovskaya et al., “Digit Ratio (2D:4D), Aggression, and Dominance in the Hadza and the Datoga of Tanzania,” Am J Human Biology 27 (2015): 620;