Behave: The Biology of Humans at Our Best and Worst

by Robert M. Sapolsky

  36.M. M. Littlefield et al., “Being Asked to Tell an Unpleasant Truth About Another Person Activates Anterior Insula and Medial Prefrontal Cortex,” Front Hum Nsci 9 (2015): 553; Footnote: S. Harris, Lying. Four Elephants Press, 2013. e-book.

  37.For a tour of animal deception, see the following: B. C. Wheeler, “Monkeys Crying Wolf? Tufted Capuchin Monkeys Use Anti-predator Calls to Usurp Resources from Conspecifics,” Proc Royal Soc B Biol Sci 276 (2009): 3013; F. Amici et al., “Variation in Withholding of Information in Three Monkey Species,” Proc Royal Soc B Biol Sci 276 (2009): 3311; A. le Roux et al., “Evidence for Tactical Concealment in a Wild Primate,” Nat Communications 4 (2013): 1462; A. Whiten and R. W. Byrne, “Tactical Deception in Primates,” BBS 11 (1988): 233; F. de Waal, Chimpanzee Politics: Power and Sex Among Apes (Baltimore, MD: Johns Hopkins University Press, 1982); G. Woodruff and D. Premack, “Intentional Communication in the Chimpanzee: The Development of Deception,” Cog 7 (1979): 333; R. W. Byrne and N. Corp, “Neocortex Size Predicts Deception Rate in Primates,” Proc Royal Soc B Biol Sci 271 (2004): 693; C. A. Ristau, “Language, Cognition, and Awareness in Animals?” ANYAS 406 (1983): 170; T. Bugnyar and K. Kotrschal, “Observational Learning and the Raiding of Food Caches in Ravens, Corvus corax: Is It ‘Tactical’ Deception?” Animal Behav 64 (2002): 185; J. Bro-Jorgensen and W. M. Pangle, “Male Topi Antelopes Alarm Snort Deceptively to Retain Females for Mating,” Am Nat 176 (2010): E33; C. Brown et al., “It Pays to Cheat: Tactical Deception in a Cephalopod Social Signalling System,” Biol Lett 8 (2012): 729; T. Flower, “Fork-Tailed Drongos Use Deceptive Mimicked Alarm Calls to Steal Food,” Proc Royal Soc B Biol Sci 278 (2011): 1548.

  38.K. G. Volz et al., “The Neural Basis of Deception in Strategic Interactions,” Front Behav Nsci 9 (2015): 27.

  39.Y. Yang et al., “Prefrontal White Matter in Pathological Liars,” Br J Psychiatry 187 (2005): 325; Y. Yang et al., “Localisation of Increased Prefrontal White Matter in Pathological Liars,” Br J Psychiatry 190 (2007):174.

  40.D. D. Langleben et al., “Telling Truth from Lie in Individual Subjects with Fast Event-Related fMRI,” Hum Brain Mapping 26 (2005): 262; J. M. Nunez et al., “Intentional False Responding Shares Neural Substrates with Response Conflict and Cognitive Control,” Neuroimage 25 (2005): 267; G. Ganis et al., “Neural Correlates of Different Types of Deception: An fMRI Investigation,” Cerebral Cortex 13 (2003): 830; K. L. Phan et al., “Neural Correlates of Telling Lies: A Functional Magnetic Resonance Imaging Study at 4 Tesla,” Academic Radiology 12 (2005): 164; N. Abe et al., “Dissociable Roles of Prefrontal and Anterior Cingulate Cortices in Deception,” Cerebral Cortex 16 (2006): 192; N. Abe, “How the Brain Shapes Deception: An Integrated Review of the Literature,” Neuroscientist 17 (2011): 560.

  41.A. Priori et al., “Lie-Specific Involvement of Dorsolateral Prefrontal Cortex in Deception,” Cerebral Cortex 18 (2008): 451; L. Zhu et al., “Damage to Dorsolateral Prefrontal Cortex Affects Tradeoffs Between Honesty and Self-Interest,” Nat Nsci 17 (2014): 1319.

  42.T. Baumgartner et al., “The Neural Circuitry of a Broken Promise,” Neuron 64 (2009): 756.

  43.Footnote: F. Sellal et al., “‘Pinocchio Syndrome’: A Peculiar Form of Reflex Epilepsy?” J Neurol, Neurosurgery and Psychiatry 56 (1993): 936.

  44.J. D. Greene and J. M. Paxton, “Patterns of Neural Activity Associated with Honest and Dishonest Moral Decisions,” PNAS 106 (2009): 12506.

  45.L. Pascual et al., “How Does Morality Work in the Brain? A Functional and Structural Perspective of Moral Behavior,” Front Integrative Nsci 7 (2013): 65.

  46.D. G. Rand and Z. G., Epstein, “Risking Your Life Without a Second Thought: Intuitive Decision-Making and Extreme Altruism,” PLoS ONE 9, no. 10 (2014): e109687; R. W. Emerson, Essays, First Series: Heroism (1841).

  Chapter 14: Feeling Someone’s Pain, Understanding Someone’s Pain, Alleviating Someone’s Pain

  1.Great reads on this general topic by leading scientists in the field: D. Keltner et al., The Compassionate Instinct: The Science of Human Goodness (New York: W. W. Norton, 2010); R. Davidson and S. Begley, The Emotional Life of Your Brain (New York: Plume, 2012).

  2.G. Hein et al., “The Brain’s Functional Network Architecture Reveals Human Motives,” Sci 351 (2016): 1074. Also see: S. Gluth and L. Fontanesi, “Wiring the Altruistic Brain,” Sci 351 (2016): 1028.

  3.A. Whiten et al., “Imitative Learning of Artificial Fruit Processing in Children (Homo sapiens) and Chimpanzees (Pan troglodytes),” JCP 110 (1996): 3; V. Horner and A. Whiten, “Causal Knowledge and Imitation/Emulation Switching in Chimpanzees (Pan troglodytes) and Children (Homo sapiens),” Animal Cog 8 (2005): 164.

  4.D. Jeon et al., “Observational Fear Learning Involves Affective Pain System and Ca1.2. CA2 Channels in ACC,” Nat Nsci 13 (2010): 482.

  5.B. L. Warren et al., “Neurobiological Sequelae of Witnessing Stressful Events in Adult Mice,” BP 73 (2012): 7.

  6.D. J. Langford et al., “Social Modulation of Pain as Evidence for Empathy in Mice,” Sci 312 (2006): 1967.

  7.M. Tomasello and V. Amrisha, “Origins of Human Cooperation and Morality,” Ann Rev Psych 64 (2013): 231; D. Povinelli et al., review of Reaching into Thought: The Minds of the Great Apes, ed. A. E. Russon et al., TICS 2 (1998): 158.

  8.F. de Waal and A. van Roosmalen, “Reconciliation and Consolation Among Chimpanzees,” Behav Ecology and Sociobiology 5 (1979): 55; E. Palagi and G. Cordoni, “Postconflict Third-Party Affiliation in Canis lupus: Do Wolves Share Similarities with the Great Apes?” Animal Behav 78 (2009): 979; A. Cools et al., “Canine Reconciliation and Third-Party-Initiated Postconflict Affiliation: Do Peacemaking Social Mechanisms in Dogs Rival Those of Higher Primates?” Ethology 14 (2008): 53; O. Fraser and T. Bugnyar, “Do Ravens Show Consolation? Responses to Distressed Others,” PLoS ONE 5, no. 5 (2010), doi:10.1371/journal.pone.0010605; A. Seed et al., “Postconflict Third-Party Affiliation in Rooks, Corvus frugilegus,” Curr Biol 2 (2006): 152; J. Plotnik and F. de Waal, “Asian Elephants (Elephas maximus) Reassure Others in Distress,” Peer J 2 (2014), doi:10.7717/peerj.278; Z. Clay and F. de Waal, “Bonobos Respond to Distress in Others: Consolation Across the Age Spectrum,” PLoS ONE 8 (2013): e55206.

  9.J. P. Burkett et al., “Oxytocin-Dependent Consolation Behavior in Rodents,” Sci 351 (2016): 375.

  10.G. E. Rice and P. Gainer, “‘Altruism’ in the Albino Rat,” J Comp and Physiological Psych 55 (1962): 123; J. S. Mogil, “The Surprising Empathic Abilities of Rodents,” TICS 16 (2012): 143; I. Ben-Ami Bartal et al., “Empathy and Pro-social Behavior in Rats,” Sci 334 (2011): 1427–30.

  11.I. B. A. Bartal et al., “Pro-social Behavior in Rats is Modulated by Social Experience,” eLife 3 (2014): e01385.

  12.C. Lamm et al., “Meta-analytic Evidence for Common and Distinct Neural Networks Associated with Directly Experienced Pain and Empathy for Pain,” Neuroimage 54 (2011): 2492; B. C. Bernhardt and T. Singer, “The Neural Basis of Empathy,” Ann Rev Nsci 35 (2012): 1.

  13.A. Craig, “How Do You Feel? Interoception: The Sense of the Physiological Condition of the Body,” Nat Rev Nsci 3 (2002): 655; J. Kong et al., “A Functional Magnetic Resonance Imaging Study on the Neural Mechanisms of Hyperalgesic Nocebo Effect,” J Nsci 28 (2008): 13354.

  14.B. Vogt, “Pain and Emotion Interactions in Subregions of the Cingulate Gyrus,” Nat Rev Nsci 6 (2005): 533; K. Ochsner et al., “Your Pain or Mine? Common and Distinct Neural Systems Supporting the Perception of Pain in Self and Other,” SCAN 3 (2008): 144; this is the source of the Ochsner quote.

  15.N. Eisenberger et al., “Does Rejection Hurt? An fMRI Study of Social Exclusion,” Sci 302 (2003): 290; D. Pizzagalli, “Frontocingulate Dysfunction in Depression: Toward Biomarkers of Treatment Response,” Neurophyschopharmacology 36 (2011): 183.

  16.C. Lamm et al., “The Neural Substrate of Human Empathy: Effects of Perspective-Taking and
Cognitive Appraisal,” J Cog Nsci 19 (2007): 42; P. Jackson et al., “Empathy Examined Through the Neural Mechanisms Involved in Imagining How I Feel Versus How You Feel Pain,” Neuropsychologia 44 (2006): 752; M. Saarela et al., “The Compassionate Brain: Humans Detect Intensity of Pain from Another’s Face,” Cerebral Cortex 17 (2007): 230; N. Eisenberg et al., “The Relations of Emotionality and Regulation to Dispositional and Situational Empathy-Related Responding,” JPSP 66 (1994): 776; J. Burkett et al., “Oxytocin-Dependent Consolation Behavior in Rodents,” Sci 351 (2016): 6271; M. Botvinick et al., “Viewing Facial Expressions of Pain Engages Cortical Areas Involved in the Direct Experience of Pain,” Neuroimage 25 (2005): 312; C. Lamm et al., “The Neural Substrate of Human Empathy: Effects of Perspective-Taking and Cognitive Appraisal,” J Cog Nsci 19 (2007): 42; C. Lamm et al., “What Are You Feeling? Using Functional Magnetic Resonance Imaging to Assess the Modulation of Sensory and Affective Responses During Empathy for Pain,” PLoS ONE 2 (2007): e1292.

  17.D. Jeon et al., “Observational Fear Learning Involves Affective Pain System and Ca(v)1.2 Ca2+ Channels in ACC,” Nat Nsci 13 (2010): 482.

  18.A. Craig, “How Do You Feel—Now? The Anterior Insula and Human Awareness,” Nat Rev Nsci 10 (2009): 59; B. King-Casas et al., “The Rupture and Repair of Cooperation in Borderline Personality Disorder,” Sci 321 (2008): 806; M. H. Immordino-Yang et al., “Neural Correlates of Admiration and Compassion,” PNAS 106 (2009): 8021.

  19.J. Decety and K. Michalska, “Neurodevelopmental Changes in the Circuits Underlying Empathy and Sympathy from Childhood to Adulthood,” Developmental Sci 13 (2009): 886; J. Decety, “The Neuroevolution of Empathy,” ANYAS 1231 (2011): 35; this second reference is the source of the quote.

  20.E. Brueau et al., “Distinct Roles of the ‘Shared Pain’ and ‘Theory of Mind’ Networks in Processing Others’ Emotional Suffering,” Neuropsychologia 50 (2012): 219; C. Lamm et al., “How Do We Empathize with Someone Who Is Not Like Us? A Functional Magnetic Resonance Imaging Study,” J Cog Nsci 22 (2010): 362; C. Keysers et al., “Somatosensation in Social Perception,” Nat Rev Nsci 11 (2010): 417.

  21.L. Harris and S. Fiske, “Dehumanizing the Lowest of the Low: Neuroimaging Responses to Extreme Outgroups,” Psych Sci 17 (2006): 847.

  22.I. Konvalinka et al., “Synchronized Arousal Between Performers and Related Spectators in a Fire-Walking Ritual,” PNAS 108 (2011): 8514; Y. Cheng et al., “Love Hurts: An fMRI Study,” NeuroImage 51 (2010): 923.

  23.A. Avenanti et al., “Transcranial Magnetic Stimulation Highlights the Sensorimotor Side of Empathy for Pain,” Nat Nsci 8 (2005): 955; X. Xu et al., “Do You Feel My Pain? Racial Group Membership Modulates Empathic Neural Responses,” J Nsci 29 (2009): 8525; V. Mathur et al., “Neural Basis of Extraordinary Empathy and Altruistic Motivation,” NeuroImage 51 (2010): 1468; G. Hein et al., “Neural Responses to Ingroup and Outgroup Members’ Suffering Predict Individual Differences in Costly Helping,” Neuron 68 (2010): 149; E. Bruneau et al., “Social Cognition in Members of Conflict Groups: Behavioural and Neural Responses in Arabs, Israelis and South Americans to Each Other’s Misfortunes,” Philosophical Transactions of the Royal Soc B 367 (2012): 717; E. Bruneau and R. Saxe, “Attitudes Towards the Outgroup are Predicted by Activity in the Precuneus in Arabs and Israelis,” NeuroImage 52 (2010): 1704; J. Gutsell and M. Inzlicht, “Intergroup Differences in the Sharing of Emotive States: Neural Evidence of an Empathy Gap,” SCAN 10 (2011): 1093; J. Freeman et al., “The Neural Origins of Superficial and Individuated Judgments About Ingroup and Outgroup Members,” Hum Brain Mapping 31 (2010): 150.

  24.Footnote: K. Wailoo, Pain: A Political History (Baltimore, MD: Johns Hopkins University Press, 2014).

  25.C. Oveis et al., “Compassion, Pride, and Social Intuitions of Self-Other Similarity,” JPSP 98 (2010): 618; M. W. Kraus et al., “Social Class, Contextualism, and Empathic Accuracy,” Psych Sci 21 (2012): 1716; J. Stellar et al., “Class and Compassion: Socioeconomic Factors Predict Responses to Suffering,” Emotion 12 (2012): 449; P. Piff et al., “Higher Social Class Predicts Increased Unethical Behavior,” PNAS 109 (2012): 4086.

  26.J. Gutsell and M. Inzlicht, “Intergroup Differences in the Sharing of Emotive States: Neural Evidence of an Empathy Gap,” SCAN 10 (2011): 1093; H. Takahasi et al., “When Your Gain Is My Pain and Your Pain Is My Gain: Neural Correlates of Envy and Schadenfreude,” Sci 323 (2009): 890; T. Singer et al., “Empathic Neural Responses Are Modulated by the Perceived Fairness of Others,” Nat 439 (2006): 466; S. Preston and F. de Waal, “Empathy: Its Ultimate and Proximate Bases,” BBS 25 (2002): 1.

  27.C. N. Dewall et al., “Depletion Makes the Heart Grow Less Helpful: Helping as a Function of Self-Regulatory Energy and Genetic Relatedness,” PSPB 34 (2008): 1653. Mother Theresa is quoted in: P. Slovic, “‘If I Look At the Mass, I Will Never Act’: Psychic Numbing and Genocide,” Judgment and Decision Making, 2 (2007): 1. The quote has been attributed to Stalin in many places, including: L Lyons, “Looseleaf Notebook,” Washington Post, January 30, 1947.

  28.A. Jenkins and J. Mitchell, “Medial Prefrontal Cortex Subserves Diverse Forms of Self-Reflection,” Soc Nsci 6 (2011): 211.

  29.G. Di Pellegrino et al., “Understanding Motor Events: A Neurophysiological Study,” Exp Brain Res 91 (1992): 176; G. Rizzolatti et al., “Premotor Cortex and the Recognition of Motor Actions,” Cog Brain Res 3 (1996): 131; also see: P. Ferrari et al., “Mirror Neurons Responding to the Observation of Ingestive and Communicative Mouth Actions in the Ventral Premotor Cortex,” Eur J Nsci 17 (2003): 1703; G. Rizzolatti and L. Craighero, “The Mirror-Neuron System,” Ann Rev Nsci 27 (2004): 169.

  30.Footnote: P. Molenberghs et al., “Is the Mirror Neuron System Involved in Imitation? A Short Review and Meta-analysis,” Nsci and Biobehavioral Reviews 33 (2009): 975.

  31.Human MRI studies: V. Gazzola and C. Keysers, “The Observation and Execution of Actions Share Motor and Somatosensory Voxels in All Tested Subjects: Single-Subject Analyses of Unsmoothed fMRI Data,” Cerebral Cortex 19 (2009): 1239; M. Iacoboni et al., “Cortical Mechanisms of Human Imitation,” Sci 286 (1999): 2526. Single neuron recordings in humans: C. Keysers and V. Gazzola, “Social Neuroscience: Mirror Neurons Recorded in Humans,” Curr Biol 20 (2010): R353; J. Kilner and A. Neal, “Evidence of Mirror Neurons in Human Inferior Frontal Gyrus,” J Nsci 29 (2009): 10153.

  32.M. Rochat et al., “The Evolution of Social Cognition: Goal Familiarity Shapes Monkeys’ Action Understanding,” Curr Biol 18 (2008): 227; M. Lacoboni, “Grasping the Intentions of Others with One’s Own Mirror Neuron System,” PLoS Biol 3 (2005): e79.

  33.C. Catmur et al., “Sensorimotor Learning Configures the Human Mirror System,” Curr Biol 17 (2007): 1527.

  34.G. Hickok, “Eight Problems for the Mirror Neuron Theory of Action Understanding in Monkeys and Humans,” J Cog Nsci 7 (2009): 1229.

  35.V. Gallese and A. Goldman, “Mirror Neurons and the Simulation Theory,” TICS 2 (1998): 493.

  36.V. Caggiano et al., “Mirror Neurons Differentially Encode the Peripersonal and Extrapersonal Space of Monkeys,” Sci 324 (2009): 403.

  37.V. Gallese et al., “Mirror Neurons,” Perspectives on Psych Sci 6 (2011): 369.

  38.A sampling of some relevant papers: L. Oberman et al., “EEG Evidence for Mirror Neuron Dysfunction in Autism Spectrum Disorders,” Brain Res: Cog Brain Res 24 (2005): 190; M. Dapretto et al., “Understanding Emotions in Others: Mirror Neuron Dysfunction in Children with Autism Spectrum Disorders,” Nat Nsci 9 (2006): 28; I. Dinstein et al., “A Mirror Up to Nature,” Curr Biol 19 (2008): R13; A. Hamilton, “Reflecting on the Mirror Neuron System in Autism: A Systematic Review of Current Theories,” Developmental Cog Nsci 3 (2013): 91.

  39.G. Hickok, The Myth of Mirror Neurons: The Real Neuroscience of Communication and Cognition (New York: Norton, 2014).

  40.D. Freedberg and V. Gallese, “Motion, Emotion and Empathy in Estheti
c Experience,” TICS 11 (2007): 197; S. Preston and F. de Waal, “Empathy: Its Ultimate and Proximate Bases,” BBS 25 (2002); 1; J. Decety and P. Jackson, “The Functional Architecture of Human Empathy,” Behav and Cog Nsci Rev 3 (2004): 71.

  41.J. Pfeifer et al., “Mirroring Others’ Emotions Relates to Empathy and Interpersonal Competence in Children,” NeuroImage 39 (2008): 2076; V. Gallese, “The ‘Shared Manifold’ Hypothesis: From Mirror Neurons to Empathy,” J Consciousness Studies 8 (2001): 33.

  42.J. Kaplan and M. Iacoboni, “Getting a Grip on Other Minds: Mirror Neurons, Intention Understanding, and Cognitive Empathy,” Soc Nsci 1 (2006): 175.

  43.Center for Building a Culture of Empathy, “Mirror Neurons,” http://cultureofempathy.com/, no date, http://cultureofempathy.com/References/Mirror-Neurons.htm; J. Marsh, “Do Mirror Neurons Give Us Empathy?” Greater Good Newsletter, March 29, 2012; V. Ramachandran, “Mirror Neurons and Imitation Learning as the Driving Force Behind ‘the Great Leap Forward’ in Human Evolution,” Edge, May 31, 2000.

  44.Grayling is quoted in C. Jarrett, “Mirror Neurons: The Most Hyped Concept in Neuroscience?” Psychology Today, December 10, 2012, www.psychologytoday.com/blog/brain-myths/201212/mirror-neurons-the-most-hyped-concept-in-neuroscience; C. Buckley, “Why Our Hero Leapt onto the Tracks and We Might Not,” New York Times, January 7, 2007.

  45.All quotes are from Hickok, 2014, op cit. For some more analysis of the skepticism, see C. Jarrett, “A Calm Look at the Most Hyped Concept in Neuroscience: Mirror Neurons,” Wired, December 13, 2013; D. Dobbs, “Mirror Neurons: Rock Stars or Backup Singers?” News Blog, ScientificAmerican.com, December 18, 2007; B. Thomas, “What’s So Special About Mirror Neurons?” Guest Blog, ScientificAmerican.com, November 6, 2012; A. Gopnik, “Cells That Read Minds?” Slate, April 26, 2007; and “A Mirror to the World,” Economist, May 12, 2005, www.economist.com/node/3960516.

  46.L. Jamison, “Forum: Against Empathy,” Boston Review, September 10, 2014.