Behave: The Biology of Humans at Our Best and Worst

by Robert M. Sapolsky

  Chapter 4: Hours to Days Before

  1.Chemical castration as generally effective for obsessive paraphiliacs: F. Berlin, “‘Chemical Castration’ for Sex Offenders,” NEJM 336 (1997): 1030. Lack of effectiveness in “hostile” rapists: K. Peters, “Chemical Castration: An Alternative to Incarceration,” Duquesne University Law Rev 31 (1992): 307. Broad conclusion that it doesn’t work particularly well: P. Fagan, “Pedophilia,” JAMA 288 (2002): 2458. I thank Arielle Lasky for excellent assistance with this research subject.

  2.For examples of the lack of correlation in a primate species, see M. Arlet et al., “Social Factors Increase Fecal Testosterone Levels in Wild Male Gray-Cheeked Mangabeys (Lophocebus albigena),” Horm Behav 59 (2011): 605; J. Archer, “Testosterone and Human Aggression: An Evaluation of the Challenge Hypothesis,” Nsci Biobehav Rev 30 (2006): 319; the quote is here.

  3.J. Oberlander and L. Henderson, “The Sturm und Drang of Anabolic Steroid Use: Angst, Anxiety, and Aggression,” TINS 35 (2012): 382; R. Agis-Balboa et al., “Enhanced Fear Responses in Mice Treated with Anabolic Androgenic Steroids,” Neuroreport 22 (2009); 617.

  4.E. Hermans, et al., “Testosterone Administration Reduces Empathetic Behavior: A Facial Mimicry Study,” PNE 31 (2006): 859; J. Honk et al., “Testosterone Administration Impairs Cognitive Empathy in Women Depending on Second-to-Fourth Digit Ratio,” PNAS 108 (2011): 3448; P. Bos et al., “Testosterone Decreases Trust in Socially Naive Humans,” PNAS 107 (2010): 9991; P. Bos et al., “The Neural Mechanisms by Which Testosterone Acts on Interpersonal Trust,” Neuroimage 2 (2012): 730; P. Mehta and J. Beer, “Neural Mechanisms of the Testosterone-Aggression Relation: The Role of the Orbitofrontal Cortex,” J Cog Nsci 22 (2009): 2357.

  5.L. Tsai and R. Sapolsky, “Rapid Stimulatory Effects of Testosterone upon Myotubule Metabolism and Hexose Transport, as Assessed by Silicon Microphysiometry,” Aggressive Behav 22 (1996): 357; C. Rutte et al., “What Sets the Odds of Winning and Losing?” TIEE 21 (2006) 16.

  Confidence and persistence: A. Boissy and M. Bouissou, “Effects of Androgen Treatment on Behavioral and Physiological Responses of Heifers to Fear-Eliciting Situations,” Horm Behav 28 (1994): 66; R. Andrew and L. Rogers, “Testosterone, Search Behaviour and Persistence,” Nat 237 (1972): 343; J. Archer, “Testosterone and Persistence in Mice,” Animal Behav 25 (1977): 479; M. Fuxjager et al., “Winning Territorial Disputes Selectively Enhances Androgen Sensitivity in Neural Pathways Related to Motivation and Social Aggression,” PNAS 107 (2010): 12393.

  Human sports: M. Elias, “Serum Cortisol, Testosterone, and Testosterone‐Binding Globulin Responses to Competitive Fighting in Human Males,” Aggressive Behav 7 (1981): 215; A. Booth et al., “Testosterone, and Winning and Losing in Human Competition,” Horm Behav 23 (1989): 556; J. Carré and S. Putnam, “Watching a Previous Victory Produces an Increase in Testosterone Among Elite Hockey Players,” PNE 35 (2010): 475; A. Mazur et al., “Testosterone and Chess Competition,” Soc Psych Quarterly 55 (1992): 70; J. Coates and J. Herbert, “Endogenous Steroids and Financial Risk Taking on a London Trading Floor,” PNAS 105 (2008): 616.

  6.N. Wright et al., “Testosterone Disrupts Human Collaboration by Increasing Egocentric Choices,” Proc Royal Soc B (2012): 2275.

  7.P. Mehta and J. Beer, “Neural Mechanisms of the Testosterone-Aggression Relation: The Role of Orbitofrontal Cortex,” J Cog Nsci 22 (2010): 2357; G. van Wingen et al., “Testosterone Reduces Amygdala–Orbitofrontal Cortex Coupling,” PNE 35 (2010): 105; P. Bos and E. Hermans et al., “The Neural Mechanisms by Which Testosterone Acts on Interpersonal Trust,” Neuroimage 2 (2012): 730.

  8.Testosterone decreasing fear and anxiety in rodents: C. Eisenegger et al., “The Role of Testosterone in Social Interaction,” TICS 15 (2011): 263. Testosterone lessens the stress response: V. Viau, “Functional Cross-Talk Between the Hypothalamic- Pituitary-Gonadal and -Adrenal Axes,” J Neuroendocrinology 14 (2002): 506. Testosterone reduces the startle response in humans: J. van Honk et al., “Testosterone Reduces Unconscious Fear But Not Consciously Experienced Anxiety: Implications for the Disorders of Fear and Anxiety,” BP 58 (2005): 218; E. J. Hermans et al., “A Single Administration of Testosterone Reduces Fear-Potentiated Startle in Humans,” BP 59 (2006): 872.

  9.General reviews: R. Woods, “Reinforcing Aspects of Androgens,” Physiology & Behav 83 (2004): 279; A. DiMeo and R. Wood, “Circulating Androgens Enhance Sensitivity to Testosterone Self-Administration in Male Hamsters,” Pharmacology, Biochemistry & Behav 79 (2004): 383; M. Packard et al., “Rewarding Affective Properties of Intra–Nucleus Accumbens Injections of Testosterone,” Behav Nsci 111 (1997): 219.

  10.A. N. Dimeo and R. I. Wood, “ICV Testosterone Induces Fos in Male Syrian Hamster Brain,” PNE 31 (2006): 237; M. Packard et al., “Rewarding Affective Properties of Intra–Nucleus Accumbens Injections of Testosterone,” Behav Nsci 111 (1997): 219; M. Packard et al., “Expression of Testosterone Conditioned Place Preference Is Blocked by Peripheral or Intra-accumbens Injection of Alpha-flupenthixol,” Horm Behav 34 (1998) 39; M. Fuxjager et al., “Winning Territorial Disputes Selectively Enhances Androgen Sensitivity in Neural Pathways Related to Motivation and Social Aggression,” PNAS 107 (2010): 12393; A. Lacreuse et al., “Testosterone May Increase Selective Attention to Threat in Young Male Macaques,” Horm Behav 58 (2010): 854.

  11.A. Dixson and J. Herbert, “Testosterone, Aggressive Behavior and Dominance Rank in Captive Adult Male Talapoin Monkeys (Miopithecus talapoin),” Physiology & Behav 18 (1977): 539.

  12.E. Hermans et al., “Exogenous Testosterone Enhances Responsiveness to Social Threat in the Neural Circuitry of Social Aggression in Humans,” BP 63 (2008): 263; J. van Honk et al., “A Single Administration of Testosterone Induces Cardiac Accelerative Responses to Angry Faces in Healthy Young Women,” Behav Nsci 115 (2001): 238; R. Ronay and A. Galinsky, “Lex Talionis: Testosterone and the Law of Retaliation,” JESP 47 (2011): 702; P. Mehta and J. Beer, “Neural Mechanisms of the Testosterone-Aggression Relation: The Role of Orbitofrontal Cortex,” J Cog Nsci 22 (2010): 2357; P. Bos et al., “Testosterone Decreases Trust in Socially Naive Humans,” PNAS 107 (2010): 9991.

  13.K. Kendrick and R. Drewett, “Testosterone Reduces Refractory Period of Stria Terminalis Neurons in the Rat Brain,” Sci 204 (1979): 877; K. Kendrick, “Inputs to Testosterone-Sensitive Stria Terminalis Neurones in the Rat Brain and the Effects of Castration,” J Physiology 323 (1982): 437; K. Kendrick, “The Effect of Castration on Stria Terminalis Neurone Absolute Refractory Periods Using Different Antidromic Stimulation Loci,” Brain Res 248 (1982): 174; K. Kendrick, “Electrophysiological Effects of Testosterone on the Medial Preoptic-Anterior Hypothalamus of the Rat,” J Endo 96 (1983): 35; E. Hermans et al., “Exogenous Testosterone Enhances Responsiveness to Social Threat in the Neural Circuitry of Social Aggression in Humans,” BP 63 (2008): 263.

  14.J. Wingfield et al., “The ‘Challenge Hypothesis’: Theoretical Implications for Patterns of Testosterone Secretion, Mating Systems, and Breeding Strategies,” Am Naturalist 136 (1990): 829.

  15.J. Archer, “Sex Differences in Aggression in Real-World Settings: A Meta-analytic Review,” Rev of General Psych 8 (2004): 291.

  16.J. Wingfield, et al., “Avoiding the ‘Costs’ of Testosterone: Ecological Bases of Hormone-Behavior Interactions,” Brain, Behav and Evolution 57 (2001): 239; M. Sobolewski et al., “Female Parity, Male Aggression, and the Challenge Hypothesis in Wild Chimpanzees,” Primates 54 (2013): 81; R. Sapolsky, “The Physiology of Dominance in Stable Versus Unstable Social Hierarchies,” in Primate Social Conflict, ed. W. Mason and S. Mendoza (New York: SUNY Press, 1993), p. 171. P. Bernhardt et al., “Testosterone Changes During Vicarious Experiences of Winning and Losing Among Fans at Sporting Events,” Physiology & Behav 65 (1998): 59.

  17.M. Muller and R. Wrangham, “Dominance, Aggression and Testosterone in Wild Chimpanzees: A Test of the ‘Challenge’ Hypothesis,” Animal
Behav 67 (2004): 113; J. Archer, “Testosterone and Human Aggression: An Evaluation of the Challenge Hypothesis,” Nsci Biobehav Rev 30 (2006): 319.

  18.Footnote: L. Gettler et al., “Longitudinal Evidence That Fatherhood Decreases Testosterone in Human Males,” PNAS 108 (2011): 16194. S. Van Anders et al., “Baby Cries and Nurturance Affect Testosterone in Men,” Horm Behav 61 (2012): 31. J. Mascaro et al., “Testicular Volume is Inversely Correlated with Nurturing-Related Brain Activity in Human Fathers,” PNAS 110 (2013): 15746. In some primates, timing is such that males are doing some degree of paternal care of offspring at the same time as doing the male-male competition thing to enhance their future reproductive success. Things get complicated here in that the paternalism and the competition should have opposite effects on testosterone levels. In the one study of this, groin trumped paternalism—testosterone levels were elevated. P. Onyango et al., “Testosterone Positively Associated with Both Male Mating Effort and Paternal Behavior in Savanna Baboons (Papio cynocephalus),” Horm Behav 63 (2012): 430.

  19.J. Higley et al., “CSF Testosterone and 5-HIAA Correlate with Different Types of Aggressive Behaviors,” BP 40 (1996): 1067.

  20.C. Eisenegger et al., “Prejudice and Truth About the Effect of Testosterone on Human Bargaining Behaviour,” Nat 463 (2010): 356.

  21.M. Wibral et al., “Testosterone Administration Reduces Lying in Men,” PLoS ONE 7 (2012): e46774. Also see: J. Van Honk et al., “New Evidence on Testosterone and Cooperation,” Nat 485 (2012): E4.

  22.Some reviews: O. Bosch and I. Neumann, “Both Oxytocin and Vasopressin Are Mediators of Maternal Care and Aggression in Rodents: From Central Release to Sites of Action,” Horm Behav 61 (2012): 293; R. Feldman, “Oxytocin and Social Affiliation in Humans,” Horm Behav 61 (2012): 380; A. Marsh et al., “The Influence of Oxytocin Administration on Responses to Infant Faces and Potential Moderation by OXTR Genotype,” Psychopharmacology (Berlin) 24 (2012): 469; M. J. Bakermans-Kranenburg and M. H. van Ijzendoorn, “Oxytocin Receptor (OXTR) and Serotonin Transporter (5-HTT) Genes Associated with Observed Parenting,” SCAN 3 (2008): 128. The hypothalamic pathway that differs by sex: N. Scott et al., “A Sexually Dimorphic Hypothalamic Circuit Controls Maternal Care and Oxytocin Secretion,” Nat 525 (2016): 519.

  23.Footnote: D. Huber et al., “Vasopressin and Oxytocin Excite Distinct Neuronal Populations in the Central Amygdala,” Sci 308 (2005): 245; D. Viviani and R. Stoop, “Opposite Effects of Oxytocin and Vasopressin on the Emotional Expression of the Fear Response,” Prog Brain Res 170 (2008): 207.

  24.Y. Kozorovitskiy et al., “Fatherhood Affects Dendritic Spines and Vasopressin V1a Receptors in the Primate Prefrontal Cortex,” Nat Nsci 9 (2006): 1094; Z. Wang et al., “Role of Septal Vasopressin Innervation in Paternal Behavior in Prairie Voles,” PNAS 91 (1994): 400.

  25.A. Smith et al., “Manipulation of the Oxytocin System Alters Social Behavior and Attraction in Pair-Bonding Primates, Callithrix penicillata,” Horm Behav 57 (2010): 255; M. Jarcho et al., “Intransal VP Affects Pair Bonding and Peripheral Gene Expression in Male Callicebus cupreus,” Genes, Brain and Behav 10 (2011): 375; C. Snowdon, “Variation in Oxytocin Is Related to Variation in Affiliative Behavior in Monogamous, Pairbonded Tamarins,” Horm Behav 58 (2010); 614.

  26.Z. Donaldson and L. Young, “Oxytocin, Vasopressin, and the Neurogenetics of Sociality,” Sci 322 (2008): 900; E. Hammock and L. Young, “Microsatellite Instability Generates Diversity in Brain and Sociobehavioral Traits,” Sci 308 (2005): 1630; L. Young et al., “Increased Affiliative Response to Vasopressin in Mice Expressing the V1a Receptor from a Monogamous Vole,” Nat 400 (1999): 766; M. Lim et al., “Enhanced Partner Preference in a Promiscuous Species by Manipulating the Expression of a Single Gene,” Nat 429 (2004): 754.

  27.E. Hammock and L. Young, “Microsatellite Instability Generates Diversity in Brain and Sociobehavioral Traits,” Sci 308 (2005): 1630.

  28.I. Schneiderman et al., “Oxytocin at the First Stages of Romantic Attachment: Relations to Couples’ Interactive Reciprocity,” PNE 37 (2012): 1277.

  29.B. Ditzen, et al., “Intranasal Oxytocin Increases Positive Communication and Reduces Cortisol Levels During Couple Conflict,” BP 65 (2009): 728; D. Scheele et al., “Oxytocin Modulates Social Distance Between Males and Females,” J Nsci 32 (2012): 16074; H. Walum et al., “Genetic Variation in the Vasopressin Receptor 1a Gene Associates with Pair-Bonding Behavior in Humans,” PNAS 105 (2008): 14153; H. Walum et al., “Variation in the Oxytocin Receptor Gene Is Associated with Pair-Bonding and Social Behavior,” BP 71 (2012): 419.

  30.M. Nagasawa et al., “Oxytocin-Gaze Positive Loop and the Coevolution of Human-Dog Bonds,” Sci 348 (2015): 333.

  31.M. Yoshida, et al., “Evidence That Oxytocin Exerts Anxiolytic Effects via Oxytocin Receptor Expressed in Serotonergic Neurons in Mice,” J Nsci 29 (2009): 2259. Oxytocin working in the amygdala: D. Viviani et al., “Oxytocin Selectively Gates Fear Responses Through Distinct Outputs from the Central Nucleus,” Sci 333 (2011): 104; H. Knobloch et al., “Evoked Axonal Oxytocin Release in the Central Amygdala Attenuates Fear Response,” Neuron 73 (2012): 553; S. Rodrigues et al., “Oxytocin Receptor Genetic Variation Relates to Empathy and Stress Reactivity in Humans,” PNAS 106 (2009): 21437; M. Bakermans-Kranenburg and M. van Ijzendoorn, “Oxytocin Receptor (OXTR) and Serotonin Transporter (5-HTT) Genes Associated with Observed Parenting,” SCAN 3 (2008): 128; G. Domes et al., “Oxytocin Attenuates Amygdala Responses to Emotional Faces Regardless of Valence,” BP 62 (2007):1187; P. Kirsch, “Oxytocin Modulates Neural Circuitry for Social Cognition and Fear in Humans,” J Nsci 25 (2005): 11489; I. Labuschagne et al., “Oxytocin Attenuates Amygdala Reactivity to Fear in Generalized Social Anxiety Disorder,” Neuropsychopharmacology 35 (2010): 2403; M. Heinrichs et al., “Social Support and Oxytocin Interact to Suppress Cortisol and Subjective Responses to Psychosocial Stress,” BP 54 (2003): 1389; K. Uvnas-Moberg, “Oxytocin May Mediate the Benefits of Positive Social Interaction and Emotions,” PNE 23 (1998): 819. Carter quoted in P. S. Churchland and P. Winkielman, “Modulating Social Behavior with Oxytocin: How Does It Work? What Does It Mean?” Horm Behav 61 (2012): 392.

  Oxytocin effects on aggression: M. Dhakar et al., “Heightened Aggressive Behavior in Mice with Lifelong Versus Postweaning Knockout of the Oxytocin Receptor,” Horm Behav 62 (2012): 86; J. Winslow et al., “Infant Vocalization, Adult Aggression, and Fear Behavior of an Oxytocin Null Mutant Mouse,” Horm Behav 37 (2005): 145.

  32.M. Kosfeld et al., “Oxytocin Increases Trust in Humans,” Nat 435 (2005): 673; A. Damasio, “Brain Trust,” Nat 435 (2005): 571; S. Israel et al., “The Oxytocin Receptor (OXTR) Contributes to Prosocial Fund Allocations in the Dictator Game and the Social Value Orientations Task,” PLoS ONE 4 (2009): e5535; P. Zak et al., “Oxytocin Is Associated with Human Trustworthiness,” Horm Behav 48 (2005): 522; T. Baumgartner et al., “Oxytocin Shapes the Neural Circuitry of Trust and Trust Adaptation in Humans,” Neuron 58 (2008): 639; A. Theodoridou et al., “Oxytocin and Social Perception: Oxytocin Increases Perceived Facial Trustworthiness and Attractiveness,” Horm Behav 56 (2009): 128. A failure of replication: C. Apicella et al., “No Association Between Oxytocin Receptor (OXTR) Gene Polymorphisms and Experimentally Elicited Social Preferences,” PLoS ONE 5 (2010): e11153. Turning the other cheek: J. Filling et al., “Effects of Intranasal Oxytocin and Vasopressin on Cooperative Behavior and Associated Brain Activity in Men,” PNE 37 (2012): 447.

  33.A. Marsh et al., “Oxytocin Improves Specific Recognition of Positive Facial Expressions,” Psychopharmacology (Berlin) 209 (2010): 225; C. Unkelbach, et al., “Oxytocin Selectively Facilitates Recognition of Positive Sex and Relationship Words,” Psych Sci 19 (2008): 102; J. Barraza et al., “Oxytocin Infusion Increases Charitable Donations Regardless of Monetary Resources,” Horm Behav 60 (2011): 148; A. Kogan et al., “Thin-Slice Study of the Oxytocin Receptor Gene and the Evaluation and Expression of the Prosocial Dispo
sition,” PNAS 108 (2011): 19189; H. Tost et al., “A Common Allele in the Oxytocin Receptor Gene (OXTR) Impacts Prosocial Temperament and Human Hypothalamic-Limbic Structure and Function,” PNAS 107 (2010): 13936; R. Hurlemann et al., “Oxytocin Enhances Amygdala-Dependent, Socially Reinforced Learning and Emotional Empathy in Humans,” J Nsci 30 (2010): 4999.

  34.P. Zak et al., “Oxytocin Is Associated with Human Trustworthiness,” Horm Behav 48 (2005): 522; J. Holt-Lunstad et al., “Influence of a ‘Warm Touch’ Support Enhancement Intervention Among Married Couples on Ambulatory Blood Pressure, Oxytocin, Alpha Amylase, and Cortisol,” Psychosomatic Med 70 (2008): 976; V. Morhenn et al., “Monetary Sacrifice Among Strangers Is Mediated by Endogenous Oxytocin Release After Physical Contact,” EHB 29 (2008): 375; C. Crockford et al., “Urinary Oxytocin and Social Bonding in Related and Unrelated Wild Chimpanzees,” Proc Royal Soc B 280 (2013): 20122765.

  35.Z. Donaldson and L. Young, “Oxytocin, Vasopressin, and the Neurogenetics of Sociality,” Sci 322 (2008): 900; A. Guastella et al., “Oxytocin Increases Gaze to the Eye Region of Human Faces,” BP 63 (2008): 3; M. Gamer et al., “Different Amygdala Subregions Mediate Valence-Related and Attentional Effects of Oxytocin in Humans,” PNAS 107 (2010): 9400; C. Zink et al., “Vasopressin Modulates Social Recognition–Related Activity in the Left Temporoparietal Junction in Humans,” Translational Psychiatry 1 (2011): e3; G. Domes et al., “Oxytocin Improves ‘Mind-Reading’ in Humans,” BP 61 (2007): 731–33; U. Rimmele et al., “Oxytocin Makes a Face in Memory More Familiar,” J Nsci 29 (2009): 38; M. Fischer-Shofty et al., “Oxytocin Facilitates Accurate Perception of Competition in Men and Kinship in Women,” SCAN (2012).

  36.C. Sauer et al., “Effects of a Common Variant in the CD38 Gene on Social Processing in an Oxytocin Challenge Study: Possible Links to Autism,” Neuropsychopharmacology 37 (2012): 1474.