Behave: The Biology of Humans at Our Best and Worst

by Robert M. Sapolsky

  37.E. Hammock and L. Young, “Oxytocin, Vasopressin and Pair Bonding: Implications for Autism,” Philosophical Transactions of the Royal Soc of London B 361 (2006): 2187; A. Meyer-Lindenberg et al., “Oxytocin and Vasopressin in the Human Brain: Social Neuropeptides for Translational Medicine,” Nat Rev Nsci 12 (2011): 524; H. Yamasue et al., “Integrative Approaches Utilizing Oxytocin to Enhance Prosocial Behavior: From Animal and Human Social Behavior to Autistic Social Dysfunction,” J Nsci 32 (2012): 14109.

  38.Reviewed in A. Graustella and C. MacLeod, “A Critical Review of the Influence of Oxytocin Nasal Spray on Social Cognition in Humans: Evidence and Future Directions,” Horm Behav 61 (2012): 410.

  39.J. Bartz et al., “Social Effects of Oxytocin in Humans: Context and Person Matter,” TICS 15 (2011): 301

  40.G. Domes et al., “Effects of Intranasal Oxytocin on Emotional Face Processing in Women,” PNE 35 (2010): 83; G. De Vries, “Sex Differences in Vasopressin and Oxytocin Innervation in the Brain,” Prog Brain Res 170 (2008): 17; J. Bartz et al., “Effects of Oxytocin on Recollections of Maternal Care and Closeness,” PNAS 14 (2010): 107.

  41.M. Mikolajczak et al., “Oxytocin Not Only Increases Trust When Money Is at Stake, but Also When Confidential Information Is in the Balance,” BP 85 (2010): 182.

  42.H. Kim et al., “Culture, Distress, and Oxytocin Receptor Polymorphism (OXTR) Interact to Influence Emotional Support Seeking,” PNAS 107 (2010): 15717.

  43.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.

  44.C. Ferris and M. Potegal, “Vasopressin Receptor Blockade in the Anterior Hypothalamus Suppresses Aggression in Hamsters,” Physiology & Behav 44 (1988): 235; H. Albers, “The Regulation of Social Recognition, Social Communication and Aggression: Vasopressin in the Social Behavior Neural Network,” Horm Behav 61 (2012): 283; A. Johansson et al., “Alcohol and Aggressive Behavior in Men: Moderating Effects of Oxytocin Receptor Gene (OXTR) Polymorphisms,” Genes, Brain and Behav 11 (2012): 214; J. Winslow and T. Insel, “Social Status in Pairs of Male Squirrel Monkeys Determines the Behavioral Response to Central Oxytocin Administration,” J Nsci 11 (1991): 2032; J. Winslow et al., “A Role for Central Vasopressin in Pair Bonding in Monogamous Prairie Voles,” Nat 365 (1993): 545.

  45.T. Baumgartner et al., “Oxytocin Shapes the Neural Circuitry of Trust and Trust Adaptation in Humans,” Neuron 58 (2008): 639; C. Declerk et al., “Oxytocin and Cooperation Under Conditions of Uncertainty: The Modulating Role of Incentives and Social Information,” Horm Behav 57 (2010): 368; S. Shamay-Tsoory et al., “Intranasal Administration of Oxytocin Increases Envy and Schadenfreude (Gloating),” BP 66 (2009): 864.

  46.C. de Dreu, “Oxytocin Modulates Cooperation Within and Competition Between Groups: An Integrative Review and Research Agenda,” Horm Behav 61 (2012): 419; C. de Dreu et al., “The Neuropeptide Oxytocin Regulates Parochial Altruism in Intergroup Conflict Among Humans,” Sci 328 (2011): 1408.

  47.C. de Dreu et al., “Oxytocin Promotes Human Ethnocentrism,” PNAS 108 (2011): 1262.

  48.Footnote: S. Motta et al., “Ventral Premammillary Nucleus as a Critical Sensory Relay to the Maternal Aggression Network,” PNAS 110 (2013): 14438.

  49.J. Lonstein and S. Gammie, “Sensory, Hormonal, and Neural Control of Maternal Aggression in Laboratory Rodents,” Nsci Biobehav Rev 26 (2002): 869; S. Parmigiani et al., “Selection, Evolution of Behavior and Animal Models in Behavioral Neuroscience,” Nsci Biobehav Rev 23 (1999): 957.

  50.R. Gandelman and N. Simon, “Postpartum Fighting in the Rat: Nipple Development and the Presence of Young,” Behav and Neural Biol 29 (1980): 350; M. Erskine et al., “Intraspecific Fighting During Late Pregnancy and Lactation in Rats and Effects of Litter Removal,” Behav Biol 23 (1978): 206; K. Flannelly and E. Kemble, “The Effect of Pup Presence and Intruder Behavior on Maternal Aggression in Rats,” Bull of the Psychonomic Soc 25 (1988): 133.

  51.B. Derntl et al., “Association of Menstrual Cycle Phase with the Core Components of Empathy,” Horm Behav 63 (2013): 97.

  For a good review see C. Bodo and E. Rissman, “New Roles for Estrogen Receptor Beta in Behavior and Neuroendocrinology,” Front Neuroendocrinology 27 (2006): 217.

  52.D. Reddy, “Neurosteroids: Endogenous Role in the Human Brain and Therapeutic Potentials,” Prog Brain Res 186 (2010): 113; F. De Sousa et al., “Progesterone and Maternal Aggressive Behavior in Rats,” Behavioural Brain Res 212 (2010): 84; G. Pinna et al., “Neurosteroid Biosynthesis Regulates Sexually Dimorphic Fear and Aggressive Behavior in Mice,” Neurochemical Res 33 (2008): 1990; K. Miczek et al., “Neurosteroids, GABAA Receptors, and Escalated Aggressive Behavior,” Horm Behav 44 (2003): 242.

  53.S. Hrdy, “The ‘One Animal in All Creation About Which Man Knows the Least,’” Philosophical Transactions of the Royal Soc B 368 (2013): 20130072.

  54.The spillover idea is aired in E. Ketterson et al., “Testosterone in Females: Mediator of Adaptive Traits, Constraint on Sexual Dimorphism, or Both?” Am Naturalist 166 (2005): 585.

  55.C. Voigt and W. Goymann, “Sex-Role Reversal Is Reflected in the Brain of African Black Coucals (Centropus grillii),” Developmental Neurobiol 67 (2007): 1560; M. Peterson et al., “Testosterone Affects Neural Gene Expression Differently in Male and Female Juncos: A Role for Hormones in Mediating Sexual Dimorphism and Conflict,” PLoS ONE 8 (2013): e61784.

  56.A. Pusey and K. Schroepfer-Walker, “Female Competition in Chimpanzees,” Philosophical Transactions of the Royal Soc B 368 (2013): 20130077.

  57.J. French et al., “The Influence of Androgenic Steroid Hormones on Female Aggression in ‘Atypical’ Mammals,” Philosophical Transactions of the Royal Soc B 368 (2013): 20130084; L. Frank et al., “Fatal Sibling Aggression, Precocial Development, and Androgens in Neonatal Spotted Hyenas,” Sci 252 (1991): 702; S. Glickman et al., “Androstenedione May Organize or Activate Sex-Reversed Traits in Female Spotted Hyenas,” PNAS 84 (1987): 3444.

  58.W. Goymann et al., “Androgens and the Role of Female ‘Hyperaggressiveness’ in Spotted Hyenas,” Horm Behav 39 (2001): 83; S. Fenstemaker et al., “A Sex Difference in the Hypothalamus of the Spotted Hyena,” Nat Nsci 2 (1999): 943; G. Rosen et al., “Distribution of Vasopressin in the Forebrain of Spotted Hyenas,” J Comp Neurol 498 (2006): 80.

  59.P. Chambers and J. Hearn, “Peripheral Plasma Levels of Progesterone, Oestradiol-17β, Oestrone, Testosterone, Androstenedione and Chorionic Gonadotrophin During Pregnancy in the Marmoset Monkey, Callithrix jacchus,” J Reproduction Fertility 56 (1979): 23; C. Drea, “Endocrine Correlates of Pregnancy in the Ring-Tailed Lemur (Lemur catta): Implications for the Masculinization of Daughters,” Horm Behav 59 (2011): 417; M. Holmes et al., “Social Status and Sex Independently Influence Androgen Receptor Expression in the Eusocial Naked Mole-Rat Brain,” Horm Behav 54 (2008): 278; L. Koren et al., “Elevated Testosterone Levels and Social Ranks in Female Rock Hyrax,” Horm Behav 49 (2006): 470; C. Kraus et al., “High Maternal Androstenedione Levels During Pregnancy in a Small Precocial Mammal with Female Genital Masculinisation” (Max Planck Institute for Demographic Research Working Paper WP 2008-017, April 2008); C. Kraus et al., “Spacing Behaviour and Its Implications for the Mating System of a Precocial Small Mammal: An Almost Asocial Cavy Cavia magna,” Animal Behav 66 (2003): 225; L. Koren and E. Geffen, “Androgens and Social Status in Female Rock Hyraxes,” Animal Behav 77 (2009): 233.

  60.Footnote: DHEA and local generation of steroids within neurons: K. Soma et al., “Novel Mechanisms for Neuroendocrine Regulation of Aggression,” Front Neuroendocrinology 29 (2008): 476; K. Schmidt et al., “Neurosteroids, Immunosteroids, and the Balkanization of Endo,” General and Comp Endo 157 (2008): 266; D. Pradhan et al., “Aggressive Interactions Rapidly Increase Androgen Synthesis in the Brain During the Non-breeding Season,” Horm
Behav 57 (2010): 381.

  61.T. Johnson, “Premenstrual Syndrome as a Western Culture-Specific Disorder,” Culture, Med and Psychiatry 11 (1987): 337; L. Cosgrove and B. Riddle, “Constructions of Femininity and Experiences of Menstrual Distress,” Women & Health 38 (2003): 37.

  62.For the quote in the text, see M. Rodin, “The Social Construction of Premenstrual Syndrome,” Soc Sci & Med 35 (1992); 49. For the quote in the footnote, see: A. Kleinman, “Depression, Somaticization, and the New ‘Cross-Cultural Psychiatry,’” Social Science Med 11 (1977): 3.

  63.H. Rupp et al., “Neural Activation in the Orbitofrontal Cortex in Response to Male Faces Increases During Follicular Phase,” Horm Behav 56 (2009): 66. Mareckova K. et al. “Hormonal Contraceptives, Menstrual Cycle and Brain Response to Faces. SCAN 9 (2012): 191.

  64.A. Rapkin et al., “Menstrual Cycle and Social Behavior in Vervet Monkeys,” PNE 20 (1995): 289; E. García-Castells et al., “Changes in Social Dynamics Associated to the Menstrual Cycle in the Vervet Monkey (Cercopithecus aethiops),” Boletín de Estudios Médicos y Biológicos 37 (1989): 11; G. Mallow, “The Relationship Between Aggressive Behavior and Menstrual Cycle Stage in Female Rhesus Monkeys (Macaca mulatta),” Horm Behav 15 (1981): 259; G. Hausfater and B. Skoblic, “Perimenstrual Behavior Changes Among Female Yellow Baboons: Some Similarities to Premenstrual Syndrome (PMS) in Women,” Animal Behav 9 (1985): 165.

  65.K. Dalton, “School Girls’ Behavior and Menstruation,” Brit Med J 2 (1960): 1647; K. Dalton, “Menstruation and Crime,” Brit Med J 2 (1961): 1752; K. Dalton, “Cyclical Criminal Acts in Premenstrual Syndrome,” Lancet 2 (1980): 1070.

  66.P. Easteal, “Women and Crime: Premenstrual Issues,” Trends and Issues in Crime and Criminal Justice 31 (1991): 1–8; J. Chrisler and P. Caplan, “The Strange Case of Dr. Jekyll and Ms. Hyde: How PMS Became a Cultural Phenomenon and a Psychiatric Disorder,” Ann Rev of Sex Res 13 (2002): 274.

  67.For a general review, see R. Sapolsky, Why Zebras Don’t Get Ulcers: A Guide to Stress, Stress-Related Diseases and Coping, 3rd ed. (New York: Henry Holt, 2004).

  68.R. Sapolsky “Stress and the Brain: Individual Variability and the Inverted-U,” Nat Nsci 25 (2015): 1344.

  69.K. Roelofs et al., “The Effects of Social Stress and Cortisol Responses on the Preconscious Selective Attention to Social Threat,”BP 75 (2007): 1; K. Tully et al., “Norepinephrine Enables the Induction of Associative Long-Term Potentiation at Thalamo-Amygdala Synapses,” PNAS 104 (2007): 14146; P. Putman et al., “Cortisol Administration Acutely Reduces Threat-Selective Spatial Attention in Healthy Young Men,” Physiology & Behav 99 (2010): 294; K. Bertsch et al., “Exogenous Cortisol Facilitates Responses to Social Threat Under High Provocation,” Horm Behav 59 (2011): 428.

  70.J. Rosenkranz et al., “Chronic Stress Causes Amygdala Hyperexcitability in Rodents,” BP 67 (2010): 1128; S. Duvarci and D. Pare, “Glucocorticoids Enhance the Excitability of Principle Basolateral Amygdala Neurons,” J Nsci 27 (2007): 4482; A. Kavushansky and G. Richter-Levin, “Effects of Stress and Corticosterone on Activity and Plasticity in the Amygdala,” J Nsci Res 84 (2006): 1580; A. Kavushansky et al., “Activity and Plasticity in the CA1, the Dentate Gyrus, and the Amygdala Following Controllable Versus Uncontrollable Water Stress,” Hippocampus 16 (2006): 35; P. Rodríguez Manzanares et al., “Previous Stress Facilitates Fear Memory, Attenuates GABAergic Inhibition, and Increases Synaptic Plasticity in the Rat Basolateral Amygdala,” J Nsci 25 (2005): 8725; H. Lakshminarasimhan and S. Chattarji, “Stress Leads to Contrasting Effects on the Levels of Brain Derived Neurotrophic Factor in the Hippocampus and Amygdala,” PLoS ONE 7 (2012): e30481; S. Ghosh et al., “Functional Connectivity from the Amygdala to the Hippocampus Grows Stronger After Stress,” J Nsci 33 (2013): 7234.

  71.B. Kolber et al., “Central Amygdala Glucocorticoid Receptor Action Promotes Fear-Associated CRH Activation and Conditioning,” PNAS 105 (2008): 12004; S. Rodrigues et al., “The Influence of Stress Hormones on Fear Circuitry,” Ann Rev Nsci 32 (2009): 289; L. Shin and I. Liberzon, “The Neurocircuitry of Fear, Stress, and Anxiety Disorders,” Neuropsychopharmacology 35, no. 1 (January 2010): 169.

  72.M. Milad and G. Quirk, “Neurons in Medial Prefrontal Cortex Signal Memory for Fear Extinction,” Nat 420 (2002): 70; E. Phelps et al., “Extinction Learning in Humans: Role of the Amygdala and vmPFC,” Neuron 43 (2004): 897; J. Bremner et al., “Neural Correlates of Exposure to Traumatic Pictures and Sound in Vietnam Combat Veterans With and Without Posttraumatic Stress Disorder: A Positron Emission Tomography Study,” BP 45 (1999) 806; D. Knox et al., “Single Prolonged Stress Disrupts Retention of Extinguished Fear in Rats,” Learning & Memory 19 (2012): 43; M. Schmidt et al., “Stress-Induced Metaplasticity: From Synapses to Behavior,” Nsci 250 (2013): 112; J. Pruessner et al., “Deactivation of the Limbic System During Acute Psychosocial Stress: Evidence from Positron Emission Tomography and Functional Magnetic Resonance Imaging Studies,” BP 63 (2008): 234.

  73.A. Young et al., “The Effects of Chronic Administration of Hydrocortisone on Cognitive Function in Normal Male Volunteers,” Psychopharmacology (Berlin) 145 (1999): 260; A. Barsegyan et al., “Glucocorticoids in the Prefrontal Cortex Enhance Memory Consolidation and Impair Working Memory by a Common Neural Mechanism,” PNAS 107 (2010): 16655; A. Arnsten et al., “Neuromodulation of Thought: Flexibilities and Vulnerabilities in Prefrontal Cortical Network Synapses,” Neuron 76 (2012): 223; B. Roozendaal et al., “The Basolateral Amygdala Interacts with the Medial Prefrontal Cortex in Regulating Glucocorticoid Effects on Working Memory Impairment,” J Nsci 24 (2004): 1385; C. Liston et al., “Psychosocial Stress Reversibly Disrupts Prefrontal Processing and Attentional Control,” PNAS 106 (2008): 912.

  74.E. Dias-Ferreira et al., “Chronic Stress Causes Frontostriatal Reorganization and Affects Decision-Making,” Sci 325 (2009): 621; D. Lyons et al., “Stress-Level Cortisol Treatment Impairs Inhibitory Control of Behavior in Monkeys,” J Nsci 20 (2000): 7816; J. Kim et al., “Amygdala Is Critical for Stress-Induced Modulation of Hippocampal Long-Term Potentiation and Learning,” J Nsci 21 (2001): 5222; L. Schwabe and O. Wolf, “Stress Prompts Habit Behavior in Humans,” J Nsci 29 (2009): 7191; L. Schwabe and O. Wolf, “Socially Evaluated Cold Pressor Stress After Instrumental Learning Favors Habits over Goal-Directed Action,” PNE 35 (2010): 977; L. Schwabe and O. Wolf, “Stress-Induced Modulation of Instrumental Behavior: From Goal-Directed to Habitual Control of Action,” BBR 219 (2011): 321; L. Schwabe and O. Wolf, “Stress Modulates the Engagement of Multiple Memory Systems in Classification Learning,” J Nsci 32 (2012): 11042; L. Schwabe et al., “Simultaneous Glucocorticoid and Noradrenergic Activity Disrupts the Neural Basis of Goal-Directed Action in the Human Brain,” J Nsci 32 (2012): 10146.

  75.V. Venkatraman et al., “Sleep Deprivation Biases the Neural Mechanisms Underlying Economic Preferences,” J Nsci 31 (2011): 3712; M. Brand et al., “Decision-Making Deficits of Korsakoff Patients in a New Gambling Task with Explicit Rules: Associations with Executive Functions,” Neuropsychology 19 (2005): 267; E. Masicampo and R. Baumeister, “Toward a Physiology of Dual-Process Reasoning and Judgment: Lemonade, Willpower, and Expensive Rule-Based Analysis,” Psych Sci 19 (2008): 255.

  76.S. Preston et al., “Effects of Anticipatory Stress on Decision-Making in a Gambling Task,” Behav Nsci 121 (2007): 257; R. van den Bos et al., “Stress and Decision-Making in Humans: Performance Is Related to Cortisol Reactivity, Albeit Differently in Men and Women,” PNE 34 (2009): 1449; N. Lighthall et al., “Acute Stress Increases Sex Differences in Risk Seeking in the Balloon Analogue Risk Task,” PLoS ONE 4 (2009): e6002; N. Lighthall et al., “Gender Differences in Reward-Related Decision Processing Under Stress,” SCAN 7, no. 4 (April 2012): 476–84; P. Putman et al., “Exogenous Cortisol Acutely Influences Motivated Decision Making in Healthy Young Men,” Psychopharmacology 208 (2010): 257; P. Putman et al., “Cortisol Administration Acutely Reduces Threat-Selective Spatial Attention i
n Healthy Young Men,” Physiology & Behav 99 (2010): 294; K. Starcke et al., “Anticipatory Stress Influences Decision Making Under Explicit Risk Conditions,” Behav Nsci 122 (2008): 1352.

  77.E. Mikics et al., “Genomic and Non-genomic Effects of Glucocorticoids on Aggressive Behavior in Male Rats,” PNE 29 (2004): 618; D. Hayden-Hixson and C. Ferris, “Steroid-Specific Regulation of Agonistic Responding in the Anterior Hypothalamus of Male Hamsters,” Physiology & Behav 50 (1991): 793; A. Poole and P. Brain, “Effects of Adrenalectomy and Treatments with ACTH and Glucocorticoids on Isolation-Induced Aggressive Behavior in Male Albino Mice,” Prog Brain Res 41 (1974): 465; E. Mikics et al., “The Effect of Glucocorticoids on Aggressiveness in Established Colonies of Rats,” PNE 32 (2007): 160; R. Böhnke et al., “Exogenous Cortisol Enhances Aggressive Behavior in Females, but Not in Males,” PNE 35 (2010): 1034; K. Bertsch et al., “Exogenous Cortisol Facilitates Responses to Social Threat Under High Provocation,” Horm Behav 59 (2011): 428.

  78.S. Levine et al., “The PNE of Stress: A Psychobiological Perspective,” in Psychoneuroendocrinology, ed. S. Levine and R. Brush (New York: Academic Press, 1988), p. 181; R. Sapolsky and J. Ray, “Styles of Dominance and Their Physiological Correlates Among Wild Baboons,” Am J Primat l8 (1989): l; J. C. Ray and R. Sapolsky, “Styles of Male Social Behavior and Their Endocrine Correlates Among High-Ranking Baboons,” Am J Primat 28 (1992): 231; C. E. Virgin and R. Sapolsky, “Styles of Male Social Behavior and Their Endocrine Correlates Among Low-Ranking Baboons,” Am J Primat 42 (1997): 25.

  79.D. Card and G. Dahl, “Family Violence and Football: The Effect of Unexpected Emotional Cues on Violent Behavior,” Quarterly J Economics 126 (2011): 103.

  80.Footnote: For a study concerning the neurobiology of how stress makes healthy habits harder to maintain, see C. Cifani et al., “Medial Prefrontal Cortex Neuronal Activation and Synaptic Alterations After Stress-Induced Reinstatement of Palatable Food Seeking: A Study Using c-fos-GFP Transgenic Female Rats,” J Nsci 32 (2012): 8480.