Behave: The Biology of Humans at Our Best and Worst

by Robert M. Sapolsky

  9.R. Rosenfield, “Clinical Review: Adolescent Anovulation: Maturational Mechanisms and Implications,” J Clin Endo and Metabolism 98 (2013): 3572.

  10.D. Yurelun-Todd, “Emotional and Cognitive Changes During Adolescence,” Curr Opinion in Neurobiol 17 (2007): 251; B. Schlaggar et al., “Functional Neuroanatomical Differences Between Adults and School-Age Children in the Processing of Single Words,” Sci 296 (2002): 1476.

  11.W. Moore et al., “Facing Puberty: Associations Between Pubertal Development and Neural Responses to Affective Facial Displays,” SCAN 7 (2012): 35.

  12.D. Gee et al., “A Developmental Shift from Positive to Negative Connectivity in Human Amygdala-Prefrontal Circuitry,” J Nsci 33 (2013): 4584.

  13.K. McRae et al., “Association Between Trait Emotional Awareness and Dorsal Anterior Cingulate Activity During Emotion Is Arousal-Dependent,” Neuroimage 41 (2008): 648; W. Killgore et al., “Sex-Specific Developmental Changes in Amygdala Responses to Affective Faces,” Neuroreport 12 (2001): 427; W. Killgore and D. Yurgelun-Todd, “Unconscious Processing of Facial Affect in Children and Adolescents,” Soc Nsci 2 (2007): 28; T. Hare et al., “Biological Substrates of Emotional Reactivity and Regulation in Adolescence During an Emotional Go-Nogo Task,” BP 63 (2008): 927; T. Wager et al., “Prefrontal-Subcortical Pathways Mediating Successful Emotion Regulation,” Neuron 25 (2008): 1037; T. Hare et al., “Self-Control in Decision-Making Involves Modulation of the vmPFC Valuation System,” Sci 324 (2009): 646; C. Masten et al., “Neural Correlates of Social Exclusion During Adolescence: Understanding the Distress of Peer Rejection,” SCAN 4 (2009): 143.; Footnote: Shulman et al., “Sex Differences in the Developmental Trajectories of Impulse Control and Sensation-Seeking from Early Adolescence to Early Adulthood,” J Youth and Adolescence 44 (2013): 1

  14.G. Laviola et al., “Risk-Taking Behavior in Adolescent Mice: Psychobiological Determinants and Early Epigenetic Influence,” Nsci Biobehav Rev 27 (2003): 19; V. Reyna and F. Farley, “Risk and Rationality in Adolescent Decision Making: Implications for Theory, Practice, and Public Policy,” Psych Sci in the Public Interest 7 (2006): 1; L. Steinberg, “Risk Taking in Adolescence: New Perspectives from Brain and Behavioral Science,” Curr Dir Psych Res 16 (2007): 55; L. Steinberg, Age of Opportunity: Lessons from the New Science of Adolescence (New York: Houghton Mifflin, 2014); C. Moutsiana et al., “Human Development of the Ability to Learn from Bad News,” PNAS 110 (2013): 16396.

  15.Reviewed in A. R. Smith et al., “The Role of the Anterior Insula in Adolescent Decision Making,” Developmental Nsci 36 (2014): 196.

  16.Footnote: Shulman et al., “Sex Differences in the Developmental Trajectories of Impulse Control and Sensation-Seeking from Early Adolescence to Early Adulthood,” J Youth and Adolescence 44 (2013): 1.

  17.R. Sapolsky, “Open Season,” New Yorker, March 30, 1998, p. 57.

  18.D. Rosenberg and D. Lewis, “Changes in the Dopaminergic Innervation of Monkey Prefrontal Cortex During Late Postnatal Development: A Tyrosine Hydroxylase Immunohistochemical Study,” BP 36 (1994): 272.

  19.B. Knutson et al., “FMRI Visualization of Brain Activity During a Monetary Incentive Delay Task,” Neuroimage 12 (2000): 20; E. Barkley-Levenson and A. Galvan, “Neural Representation of Expected Value in the Adolescent Brain,” PNAS 111 (2014): 1646; S. Schneider et al., “Risk Taking and the Adolescent Reward System: A Potential Common Link to Substance Abuse,” Am J Psychiatry 169 (2012): 39; S. Burnett et al., “Development During Adolescence of the Neural Processing of Social Emotion,” J Cog Nsci 21 (2008): 1; J. Bjork et al., “Developmental Differences in Posterior Mesofrontal Cortex Recruitment by Risky Rewards,” J Nsci 27 (2007): 4839; J. Bjork et al., “Incentive-Elicited Brain Activation in Adolescents: Similarities and Differences from Young Adults,” J Nsci 25 (2004): 1793; S. Blakemore et al., “Adolescent Development of the Neural Circuitry for Thinking About Intentions,” SCAN 2 (2007): 130.

  20.A. Galvan et al., “Earlier Development of the Accumbens Relative to Orbitofrontal Cortex Might Underlie Risk-Taking Behavior in Adolescents,” J Nsci 26 (2006): 6885 (this is also the source of the figure in the text). A demonstration of dopaminergic response to different reward sizes as more linear and accurate in adults: J. Vaidya et al., “Neural Sensitivity to Absolute and Relative Anticipated Reward in Adolescents,” PLoS ONE 8 (2013): e58708.

  21.A. R. Smith et al., “Age Differences in the Impact of Peers on Adolescents’ and Adults’ Neural Response to Reward,” Developmental Cog Nsci 11 (2015): 75; J. Chein et al., “Peers Increase Adolescent Risk Taking by Enhancing Activity in the Brain’s Reward Circuitry,” Developmental Sci 14 (2011): F1; M. Gardner and L. Steinberg, “Peer Influence on Risk Taking, Risk Preference, and Risky Decision Making in Adolescence and Adulthood: An Experimental Study,” Developmental Psych 41 (2005): 625; L. Steinberg, “A Social Neuroscience Perspective on Adolescent Risk-Taking,” Developmental Rev 28 (2008): 78; M. Grosbras et al., “Neural Mechanisms of Resistance to Peer Influence in Early Adolescence,” J Nsci 27 (2007): 8040; A. Weigard et al., “Effects of Anonymous Peer Observation on Adolescents’ Preference for Immediate Rewards,” Developmental Science 17 (2014): 71.

  22.M. Madden et al., “Teens, Social Media, and Privacy,” Pew Research Center, May 23, 2013, www.pewinternet.org/Reports/2013/Teens-Social-Media-And-Privacy/Summary-of-Findings.aspx.

  23.A. Guyer et al., “Amygdala and Ventrolateral Prefrontal Cortex Function During Anticipated Peer Evaluation in Pediatric Social Anxiety,” AGP 65 (2008): 1303; A. Guyer et al., “Probing the Neural Correlates of Anticipated Peer Evaluation in Adolescence,” Child Development 80 (2009): 1000; B. Gunther Moor et al., “Do You Like Me? Neural Correlates of Social Evaluation and Developmental Trajectories,” Soc Nsci 5 (2010): 461.

  24.N. Eisenberger et al., “Does Rejection Hurt? An fMRI Study of Social Exclusion,” Sci 302 (2003): 290; N. Eisenberger, “The Pain of Social Disconnection: Examining the Shared Neural Underpinnings of Physical and Social Pain,” Nat Rev Nsci 3 (2012): 421.

  25.C. Sebastian et al., “Development Influences on the Neural Bases of Responses to Social Rejection: Implications of Social Neuroscience for Education,” NeuroImage 57 (2011): 686; C. Masten et al., “Neural Correlates of Social Exclusion During Adolescence: Understanding the Distress of Peer Rejection,” SCAN 4 (2009): 143; J. Pfeifer and S. Blakemore, “Adolescent Social Cognitive and Affective Neuroscience: Past, Present, and Future,” SCAN 7 (2012): 1.

  26.J. Pfeifer et al., “Entering Adolescence: Resistance to Peer Influence, Risky Behavior, and Neural Changes in Emotion Reactivity,” Neuron 69 (2011): 1029; L. Steinberg and K. Monahan, “Age Differences in Resistance to Peer Influence,” Developmental Psych 43 (2007): 1531; M. Grosbras et al., “Neural Mechanisms of Resistance to Peer Influence in Early Adolescence,” J Nsci 27 (2007): 8040.

  27.I. Almas et al., “Fairness and the Development of Inequality Acceptance,” Sci 328 (2010): 1176.

  28.J. Decety and K. Michalska, “Neurodevelopmental Changes in the Circuits Underlying Empathy and Sympathy from Childhood to Adulthood,” Developmental Sci 13 (2010): 886.

  29.N. Eisenberg et al., “The Relations of Emotionality and Regulation to Dispositional and Situational Empathy-Related Responding,” JPSP 66 (1994): 776; J. Decety et al., “The Developmental Neuroscience of Moral Sensitivity,” Emotion Rev 3 (2011): 305.

  30.E. Finger et al., “Disrupted Reinforcement Signaling in the Orbitofrontal Cortex and Caudate in Youths with Conduct Disorder or Oppositional Defiant Disorder and a High Level of Psychopathic Traits,” Am J Psychiatry 168 (2011): 152; A. Marsh et al., “Reduced Amygdala-Orbitofrontal Connectivity During Moral Judgments in Youths with Disruptive Behavior Disorders and Psychopathic Traits,” Psychiatry Res 194 (2011): 279.

  31.L. Steinberg, “The Influence of Neuroscience on US Supreme Court Decisions About Adolescents’ Criminal Culpability,” Nat Rev Nsci 14 (2013): 513.
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  32.Roper v. Simmons, 543 U.S. 551 (2005).

  33.J. Sallet et al, “Social Network Size Affects Neural Circuits in Macaques,” Sci 334 (2011): 697.

  Chapter 7: Back to the Crib, Back to the Womb

  1.P. Yakovlev and A. Lecours, “The Myelogenetic Cycles of Regional Maturation of the Brain,” in Regional Development of the Brain in Early Life, ed. A. Minkowski (Oxford: Blackwell, 1967); H. Kinney et al., “Sequence of Central Nervous System Myelination in Human Infancy: II. Patterns of Myelination in Autopsied Infants,” J Neuropathology & Exp Neurol 47 (1988): 217; S. Deoni et al., “Mapping Infant Brain Myelination with MRI,” J Nsci 31 (2011): 784; N. Baumann and D. Pham-Dinh, “Biology of Oligodendrocyte and Myelin in the Mammalian CNS,” Physiological Rev 81 (2001): 871.

  2.Demonstration of the predictive power of degree of connectivity: N. Dosenbach et al., “Prediction of Individual Brain Maturity Using fMRI,” Sci 329 (2010): 1358.

  3.N. Uesaka et al., “Retrograde Semaphorin Signaling Regulates Synapse Elimination in the Developing Mouse Brain,” Sci 344 (2014): 1020; R. C. Paolicelli et al., “Synaptic Pruning by Microglia Is Necessary for Normal Brain Development,” Sci 333 (2011): 1456; R. Buss et al., “Adaptive Roles of Programmed Cell Death During Nervous System Development,” Ann Rev of Nsci 29 (2006): 1; D. Nijhawan et al., “Apoptosis in Neural Development and Disease,” Ann Rev of Nsci 23 (2000): 73; C. Kuan et al., “Mechanisms of Programmed Cell Death in the Developing Brain,” TINS 23 (2000): 291.

  4.J. Piaget, Main Trends in Psychology (London: George Allen & Unwin, 1973); J. Piaget, The Language and Thought of the Child (New York: Psychology Press, 1979).

  5.Other realms of stage development: R. Selman et al., “Interpersonal Awareness in Children: Toward an Integration of Developmental and Clinical Child Psychology,” Am J Orthopsychiatry 47 (1977): 264; T. Singer, “The Neuronal Basis and Ontogeny of Empathy and Mind Reading: Review of Literature and Implications for Future Research,” Nsci Biobehav Rev 30 (2006): 855.

  6.S. Baron-Cohen, “Precursors to a Theory of Mind: Understanding Attention in Others,” in Natural Theories of Mind: Evolution, Development and Simulation of Everyday Mindreading, ed. A. Whiten (Oxford: Basil Blackwell, 1991); J. Topal et al., “Differential Sensitivity to Human Communication in Dogs, Wolves, and Human Infants,” Sci 325 (2009): 1269; G. Lakatos et al., “A Comparative Approach to Dogs’ (Canis familiaris) and Human Infants’ Comprehension of Various Forms of Pointing Gestures,” Animal Cog 12 (2009): 621 J. Kaminski et al., “Domestic Dogs are Sensitive to a Human’s Perspective,” Behaviour 146 (2009): 979.

  7.S. Baron-Cohen et al., “Does the Autistic Child Have a ‘Theory of Mind’?” Cog 21 (2985): 37.

  8.L. Young et al., “Disruption of the Right Temporal Lobe Function with TMS Reduces the Role of Beliefs in Moral Judgments,” PNAS 107 (2009): 6753; Y. Moriguchi et al., “Changes of Brain Activity in the Neural Substrates for Theory of Mind During Childhood and Adolescence,” Psychiatry and Clin Nsci 61 (2007): 355; A. Saitovitch et al., “Social Cognition and the Superior Temporal Sulcus: Implications in Autism,” Rev of Neurol (Paris) 168 (2012): 762; P. Shaw et al., “The Impact of Early and Late Damage to the Human Amygdala on ‘Theory of Mind’ Reasoning,” Brain 127 (2004): 1535.

  9.B. Sodian and S. Kristen, “Theory of Mind During Infancy and Early Childhood Across Cultures, Development of,” Int Encyclopedia of the Soc & Behav Sci (Amsterdam: Elsevier, 2015), p. 268.

  10.S. Nichols, “Experimental Philosophy and the Problem of Free Will,” Sci 331 (2011): 1401.

  11.D. Premack and G. Woodruff, “Does the Chimpanzee Have a Theory of Mind?” BBS 1 (1978): 515. Evidence against: D. Povinelli and J. Vonk, “Chimpanzee Minds: Suspiciously Human?” TICS 7 (2003): 157. Evidence for: B. Hare et al., “Do Chimpanzees Know What Conspecifics Know and Do Not Know?” Animal Behav 61 (2001): 139. Footnote: L. Santo Let al., “Rhesus Monkeys (Macaca mulatta) Know What Others Can and Cannot Hear,” Animal Behav 71 (2006): 1175.

  12.J. Decety et al., “The Contribution of Emotion and Cognition to Moral Sensitivity: A Neurodevelopmental Study,” Cerebral Cortex 22 (2011): 209.

  13.J. Decety et al., “Who Caused the Pain? An fMRI Investigation of Empathy and Intentionality in Children,” Neuropsychologia 46 (2008): 2607; J. Decety et al., “The Contribution of Emotion and Cognition to Moral Sensitivity: A Neurodevelopmental Study,” Cerebral Cortex 22 (2012): 209; J. Decety and K. Michalska, “Neurodevelopmental Changes in the Circuits Underlying Empathy and Sympathy from Childhood to Adulthood,” Developmental Sci 13 (2010): 886.

  14.J. Decety et al., “The Contribution of Emotion and Cognition to Moral Sensitivity: A Neurodevelopmental Study,” Cerebral Cortex 22 (2012): 209; N. Eisenberg et al., “The Relations of Emotionality and Regulation to Dispositional and Situational Empathy-Related Responding,” JPSP 66 (1994): 776.

  15.P. Blake et al., “The Ontogeny of Fairness in Seven Societies,” Nat 528 (2016): 258.

  16.I. Almas et al., “Fairness and the Development of Inequality Acceptance,” Sci 328 (2010): 1176; E. Fehr et al., “Egalitarianism in Young Children,” Nat 454 (2008): 1079; K. Olson et al., “Children’s Responses to Group-Based Inequalities: Perpetuation and Rectification,” Soc Cog 29 (2011): 270; M. Killen, “Children’s Social and Moral Reasoning About Exclusion,” Curr Dir Psych Sci 16 (2007): 32.

  17.D. Garz, Lawrence Kohlberg: An Introduction (Cologne, Germany: Barbara Budrich, 2009).

  18.C. Gilligan, In a Different Voice: Psychological Theory and Women’s Development (Cambridge, MA: Harvard University Press, 1982).

  19.N. Eisenberg, “Emotion, Regulation, and Moral Development,” Ann Rev of Psych 51 (2000): 665; J. Hamlin et al., “Social Evaluation by Preverbal Infants,” Nat 450 (2007): 557; M. Hoffman, Empathy and Moral Development: Implications for Caring and Justice (Cambridge: Cambridge University Press, 2001).

  20.W. Mischel et al., “Cognitive and Attentional Mechanisms in Delay of Gratification,” JPSP 21 (1972): 204; W. Mischel, The Marshmallow Test: Understanding Self-Control and How to Master It (New York: Bantam Books, 2014); K. McRae et al., “The Development of Emotion Regulation: An fMRI Study of Cognitive Reappraisal in Children, Adolescents and Young Adults,” SCAN 7 (2012): 11; H. Palmeri and R. N. Aslin, “Rational Snacking: Young Children’s Decision-Making on the Marshmallow Task is Moderated by Beliefs About Environmental Reliability,” Cog 126 (2013): 109.

  21.B. J. Casey et al., “From the Cover: Behavioral and Neural Correlates of Delay of Gratification 40 Years Later,” PNAS 108 (2011): 14998; N. Eisenberg et al., “Contemporaneous and Longitudinal Prediction of Children’s Social Functioning from Regulation and Emotionality,” Child Development 68 (1997): 642; N. Eisenberg et al., “The Relations of Regulation and Emotionality to Resiliency and Competent Social Functioning in Elementary School Children,” Child Development 68 (1997): 295.

  22.L. Holt, The Care and Feeding of Children (NY: Appleton-Century, 1894). This book went through fifteen editions between 1894 and 1915.

  23.For a history of hospitalism, see R. Sapolsky, “How the Other Half Heals,” Discover, April 1998, p. 46.

  24.J. Bowlby Attachment and Loss, vol. 1, Attachment (New York: Basic Books, 1969); J. Bowlby, Attachment and Loss, vol. 2, Separation (London: Hogarth Press, 1973); J. Bowlby, Attachment and Loss, vol. 3, Loss: Sadness & Depression (London: Hogarth Press, 1980).

  25.D. Blum, Love at Goon Park: Harry Harlow and the Science of Affection (New York: Perseus, 2002). This is the source of the Harlow quote.

  26.R. Rosenfeld, “The Case of the Unsolved Crime Decline,” Sci Am, February 2004, p. 82; J. Donohue III and S. Levitt, “The Impact of Legalized Abortion on Crime,” Quarterly J Economics 116 (2001): 379. Raine et al., “Birth Complications Combined with Early Maternal Rejection at Age 1 Year Predispose to Violent Crime at Age 18 Years,” AGP 51 (1994): 984; Footnote: J. Bowlby, “Forty-f
our Juvenile Thieves: Their Characters and Home-Life,” Int J Psychoanalysis 25 (1944): 107.

  27.G. Barr et al., “Transitions in Infant Learning Are Modulated by Dopamine in the Amygdala,” Nat Nsci 12 (2009): 1367; R. Sullivan et al., “Good Memories of Bad Events,” Nat 407 (2000): 38; S. Moriceau et al., “Dual Circuitry for Odor-Shock Conditioning During Infancy: Corticosterone Switches Between Fear and Attraction via Amygdala,” J Nsci 26 (2006): 6737; R. Sapolsky, “Any Kind of Mother in a Storm,” Nat Nsci 12 (2009): 1355.

  28.R. Sapolsky and M. Meaney, “Maturation of the Adrenocortical Stress Response: Neuroendocrine Control Mechanisms and the Stress Hyporesponsive Period,” Brain Res Rev 11 (1986): 65.

  29.L. M. Renner and K. S. Slack, “Intimate Partner Violence and Child Maltreatment: Understanding Intra- and Intergenerational Connections,” Child Abuse & Neglect 30 (2006): 599.

  30.D. Maestripieri, “Early Experience Affects the Intergenerational Transmission of Infant Abuse in Rhesus Monkeys,” PNAS 102 (2005): 9726.

  31.C. Hammen et al., “Depression and Sensitization to Stressors Among Young Women as a Function of Childhood Adversity,” J Consulting Clin Psych 68 (2000): 782; E. McCrory et al., “The Link Between Child Abuse and Psychopathology: A Review of Neurobiological and Genetic Research,” J the Royal Soc of Med 105 (2012): 151; K. Lalor and R. McElvaney, “Child Sexual Abuse, Links to Later Sexual Exploitation/High-Risk Sexual Behavior, and Prevention/Treatment Programs,” Trauma Violence & Abuse 11 (2010): 159; Y. Dvir et al., “Childhood Maltreatment, Emotional Dysregulation, and Psychiatric Comorbidities,” Harvard Rev of Psychiatry 22 (2014): 149; E. Mezzacappa et al., “Child Abuse and Performance Task Assessments of Executive Functions in Boys,” J Child Psych and Psychiatry 42 (2001): 1041; M. Wichers et al., “Transition from Stress Sensitivity to a Depressive State: Longitudinal Twin Study,” Brit J Psychiatry 195 (2009): 498.