Neural mechanisms of social decision-making in the primate amygdala

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 52, 2015, Pages 16012-16017

  Chang, Steve W C ^a,b   Fagan, Nicholas A ^a   Toda, Koji ^c,d   Utevsky, Amanda V ^c   Pearson, John M ^c   Platt, Michael L ^c,e,f,g   Gazzaniga, Michael S ^h  

^a YALE UNIVERSITY   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d JAPAN SOCIETY FOR THE PROMOTION OF SCIENCE   (Japan)

^e UNIVERSITY OF PENNSYLVANIA   (United States)

^f UNIVERSITY OF PENNSYLVANIA   (United States)

^g UNIVERSITY OF PENNSYLVANIA   (United States)

^h UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

OXYTOCIC AGENT; OXYTOCIN;

ANIMAL; ASSOCIATION; BASOLATERAL AMYGDALA; BIOLOGICAL MODEL; CYTOLOGY; DECISION MAKING; DRUG EFFECTS; HUMAN; MARKOV CHAIN; MONTE CARLO METHOD; NERVE CELL; NERVE TRACT; PHYSIOLOGY; PSYCHOLOGY; REWARD; RHESUS MONKEY; SOCIAL BEHAVIOR;

ANIMALS; BASOLATERAL NUCLEAR COMPLEX; CHOICE BEHAVIOR; CUES; DECISION MAKING; HUMANS; MACACA MULATTA; MARKOV CHAINS; MODELS, NEUROLOGICAL; MONTE CARLO METHOD; NEURAL PATHWAYS; NEURONS; OXYTOCICS; OXYTOCIN; REWARD; SOCIAL BEHAVIOR;

EID: 84953232757     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1514761112     Document Type: Article

References (67)

1. Singer T, et al. (2006) Empathic neural responses are modulated by the perceived fairness of others. Nature 439(7075):466-469.
2. Fehr E, Fischbacher U (2003) The nature of human altruism. Nature 425(6960):785-791.
3. de Waal FBM (2008) Putting the altruism back into altruism: The evolution of empathy. Annu Rev Psychol 59:279-300.
4. Behrens TEJ, Hunt LT, Rushworth MFS (2009) The computation of social behavior. Science 324(5931):1160-1164.
5. Chang SWC, et al. (2013) Neuroethology of primate social behavior. Proc Natl Acad Sci USA 110(Suppl 2):10387-10394.
6. Carter RM, Bowling DL, Reeck C, Huettel SA (2012) A distinct role of the temporal- parietal junction in predicting socially guided decisions. Science 337(6090):109-111.
7. Chang SWC, Gariépy JF, Platt ML (2013) Neuronal reference frames for social decisions in primate frontal cortex. Nat Neurosci 16(2):243-250.
8. Yoshida K, Saito N, Iriki A, Isoda M (2011) Representation of others' action by neurons in monkey medial frontal cortex. Curr Biol 21(3):249-253.
9. Azzi JCB, Sirigu A, Duhamel JR (2012) Modulation of value representation by social context in the primate orbitofrontal cortex. Proc Natl Acad Sci USA 109(6):2126-2131.
10. Haroush K, Williams ZM (2015) Neuronal prediction of opponent's behavior during cooperative social interchange in primates. Cell 160(6):1233-1245.
11. Báez-Mendoza R, Harris CJ, SchultzW (2013) Activity of striatal neurons reflects social action and own reward. Proc Natl Acad Sci USA 110(41):16634-16639.
12. Cardinal RN, Parkinson JA, Hall J, Everitt BJ (2002) Emotion and motivation: The role of the amygdala, ventral striatum, and prefrontal cortex. Neurosci Biobehav Rev 26(3):321-352.
13. Gallagher M, Chiba AA (1996) The amygdala and emotion. Curr Opin Neurobiol 6(2): 221-227.
14. Kluver H, Bucy PC (1939) Preliminary analysis of functions of the temporal lobes in monkeys. Arch Neurol Psychiatry 42(6):979-1000.
15. LeDoux JE (2000) Emotion circuits in the brain. Annu Rev Neurosci 23(1):155-184.
16. Morris JS, et al. (1996) A differential neural response in the human amygdala to fearful and happy facial expressions. Nature 383(6603):812-815.
17. Phelps EA (2006) Emotion and cognition: Insights from studies of the human amygdala. Annu Rev Psychol 57:27-53.
18. Paton JJ, Belova MA, Morrison SE, Salzman CD (2006) The primate amygdala represents the positive and negative value of visual stimuli during learning. Nature 439(7078):865-870.
19. De Martino B, Camerer CF, Adolphs R (2010) Amygdala damage eliminates monetary loss aversion. Proc Natl Acad Sci USA 107(8):3788-3792.
20. Hernádi I, Grabenhorst F, Schultz W (2015) Planning activity for internally generated reward goals in monkey amygdala neurons. Nat Neurosci 18(3):461-469.
21. DavisM,Whalen PJ (2001) The amygdala: Vigilance and emotion. Mol Psychiatry 6(1):13-34.
22. Gallagher HL, Frith CD (2003) Functional imaging of 'theory of mind'. Trends Cogn Sci 7(2):77-83.
23. Mars RB, Sallet J, Neubert FX, Rushworth MFS (2013) Connectivity profiles reveal the relationship between brain areas for social cognition in human and monkey temporoparietal cortex. Proc Natl Acad Sci USA 110(26):10806-10811.
24. Adolphs R (2010) What does the amygdala contribute to social cognition? Ann N Y Acad Sci 1191(1):42-61.
25. Mosher CP, Zimmerman PE, Gothard KM (2014) Neurons in the monkey amygdala detect eye contact during naturalistic social interactions. Curr Biol 24(20):2459-2464.
26. Gothard KM, Battaglia FP, Erickson CA, Spitler KM, Amaral DG (2007) Neural responses to facial expression and face identity in the monkey amygdala. J Neurophysiol 97(2): 1671-1683.
27. Donaldson ZR, Young LJ (2008) Oxytocin, vasopressin, and the neurogenetics of sociality. Science 322(5903):900-904.
28. Kirsch P, et al. (2005) Oxytocin modulates neural circuitry for social cognition and fear in humans. J Neurosci 25(49):11489-11493.
29. Petrovic P, Kalisch R, Singer T, Dolan RJ (2008) Oxytocin attenuates affective evaluations of conditioned faces and amygdala activity. J Neurosci 28(26):6607-6615.
30. Liu N, et al. (2015) Oxytocin modulates fMRI responses to facial expression in macaques. Proc Natl Acad Sci USA 112(24):E3123-E3130.
31. Gamer M, Zurowski B, Büchel C (2010) Different amygdala subregions mediate valence- related and attentional effects of oxytocin in humans. Proc Natl Acad Sci USA 107(20):9400-9405.
32. Gordon I, et al. (2013) Oxytocin enhances brain function in children with autism. Proc Natl Acad Sci USA 110(52):20953-20958.
33. Chang SWC, Barter JW, Ebitz RB, Watson KK, Platt ML (2012) Inhaled oxytocin amplifies both vicarious reinforcement and self reinforcement in rhesus macaques (Macaca mulatta). Proc Natl Acad Sci USA 109(3):959-964.
34. Chang SWC, Winecoff AA, Platt ML (2011) Vicarious reinforcement in rhesus macaques (macaca mulatta). Front Neurosci 5:27.
35. Damon W, Lerner RM, Eisenberg N, eds (2006) Handbook of Child Psychology. Vol. 3: Social, Emotional, and Personality Development (Wiley, Hoboken, NJ), 6th Ed.
36. Brief AP, Motowidlo SJ (1986) Prosocial organizational behaviors. Acad Manage Rev 11(4):710-725.
37. Penner LA, Dovidio JF, Piliavin JA, Schroeder DA (2005) Prosocial behavior: Multilevel perspectives. Annu Rev Psychol 56:365-392.
38. Batson CD, Powell AA (2003) Altruism and prosocial behavior. Handbook of Psychology. Part 3: Social Psychology (Wiley, New York), pp 463-484.
39. Bandura A, Ross D, Ross SA (1963) Vicarious reinforcement and imitative learning. J Abnorm Psychol 67:601-607.
40. Peck CJ, Lau B, Salzman CD (2013) The primate amygdala combines information about space and value. Nat Neurosci 16(3):340-348.
41. Domes G, et al. (2007) Oxytocin attenuates amygdala responses to emotional faces regardless of valence. Biol Psychiatry 62(10):1187-1190.
42. RiemMME, et al. (2011) Oxytocinmodulates amygdala, insula, and inferior frontal gyrus responses to infant crying: A randomized controlled trial. Biol Psychiatry 70(3):291-297.
43. Labuschagne I, et al. (2010) Oxytocin attenuates amygdala reactivity to fear in generalized social anxiety disorder. Neuropsychopharmacology 35(12):2403-2413.
44. Domes G, et al. (2010) Effects of intranasal oxytocin on emotional face processing in women. Psychoneuroendocrinology 35(1):83-93.
45. Lischke A, et al. (2012) Oxytocin increases amygdala reactivity to threatening scenes in females. Psychoneuroendocrinology 37(9):1431-1438.
46. Freeman SM, Inoue K, Smith AL, Goodman MM, Young LJ (2014) The neuroanatomical distribution of oxytocin receptor binding and mRNA in the male rhesus macaque (Macaca mulatta). Psychoneuroendocrinology 45:128-141.
47. Owen SF, et al. (2013) Oxytocin enhances hippocampal spike transmission by modulating fast-spiking interneurons. Nature 500(7463):458-462.
48. Gallese V, Keysers C, Rizzolatti G (2004) A unifying view of the basis of social cognition. Trends Cogn Sci 8(9):396-403.
49. Rizzolatti G, Craighero L (2004) Themirror-neuron system. Annu Rev Neurosci 27(1):169-192.
50. Tomlin D, et al. (2006) Agent-specific responses in the cingulate cortex during economic exchanges. Science 312(5776):1047-1050.
51. Mitchell JP, Macrae CN, Banaji MR (2006) Dissociable medial prefrontal contributions to judgments of similar and dissimilar others. Neuron 50(4):655-663.
52. Singer T, et al. (2004) Empathy for pain involves the affective but not sensory components of pain. Science 303(5661):1157-1162.
53. McClure SM, York MK, Montague PR (2004) The neural substrates of reward processing in humans: The modern role of FMRI. Neuroscientist 10(3):260-268.
54. O'Doherty JP (2004) Reward representations and reward-related learning in the human brain: insights from neuroimaging. Curr Opin Neurobiol 14(6):769-776.
55. Morrison SE, Salzman CD (2010) Re-valuing the amygdala. Curr Opin Neurobiol 20(2): 221-230.
56. Amaral DG (2003) The amygdala, social behavior, and danger detection. Ann N Y Acad Sci 1000(1):337-347.
57. Baxter MG, Murray EA (2002) The amygdala and reward. Nat Rev Neurosci 3(7):563-573.
58. Carmichael ST, Price JL (1995) Limbic connections of the orbital and medial prefrontal cortex in macaque monkeys. J Comp Neurol 363(4):615-641.
59. Fudge JL, Kunishio K, Walsh P, Richard C, Haber SN (2002) Amygdaloid projections to ventromedial striatal subterritories in the primate. Neuroscience 110(2):257-275.
60. Russchen FT, Bakst I, Amaral DG, Price JL (1985) The amygdalostriatal projections in the monkey. An anterograde tracing study. Brain Res 329(1-2):241-257.
61. Decety J, Jackson PL (2006) A social-neuroscience perspective on empathy. Curr Dir Psychol Sci 15(2):54-58.
62. Engen HG, Singer T (2013) Empathy circuits. Curr Opin Neurobiol 23(2):275-282.
63. Brainard DH (1997) The Psychophysics Toolbox. Spat Vis 10(4):433-436.
64. Kawashima R, et al. (1999) The human amygdala plays an important role in gaze monitoring: A PET study. Brain 122(4):779-783.
65. Adolphs R, et al. (2005) A mechanism for impaired fear recognition after amygdala damage. Nature 433(7021):68-72.
66. Whalen PJ, et al. (1998) Masked presentations of emotional facial expressions modulate amygdala activity without explicit knowledge. J Neurosci 18(1):411-418.
67. Hoffman KL, Gothard KM, Schmid MC, Logothetis NK (2007) Facial-expression and gaze-selective responses in the monkey amygdala. Curr Biol 17(9):766-772.