Social learning of fear

Nature Neuroscience

Volumn 10, Issue 9, 2007, Pages 1095-1102

  Olsson, Andreas ^a   Phelps, Elizabeth A ^b  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b NEW YORK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYGDALOID NUCLEUS; CONDITIONING; EXPLICIT MEMORY; FEAR; HUMAN; NONHUMAN; PRIORITY JOURNAL; REVIEW; SOCIAL BEHAVIOR; SOCIAL LEARNING;

AMYGDALA; ANIMALS; ASSOCIATION LEARNING; AVOIDANCE LEARNING; EMOTIONS; FEAR; HUMANS; MODELS, BIOLOGICAL; SOCIAL BEHAVIOR;

EID: 34548324246     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn1968     Document Type: Review

References (100)

1. Pavlov, I.P. Conditioned Reflexes (Oxford Univ. Press, Oxford, 1927).
2. Phelps, E.A. & LeDoux, J.E. Contributions of the amygdala to emotion processing: from animal models to human behavior. Neuron 48, 175-187 (2005).
3. Amaral, D.G. Amygdalohippocampal and amygdalocortical projections in the primate brain. Adv. Exp. Med. Biol. 203, 3-17 (1986).
4. LeDoux, J.E., Farb, C. & Ruggiero, D.A. Topographic organization of neurons in the acoustic thalamus that project to the amygdala. J. Neurosci. 10, 1043-1054 (1990).
5. Romanski, L.M., Clugnet, M.C., Bordi, F. & LeDoux, J.E. Somatosensory and auditory convergence in the lateral nucleus of the amygdala. Behav. Neurosci. 107, 444-450 (1993).
6. Quirk, G.J., Armony, J.L. & LeDoux, J.E. Fear conditioning enhances different temporal components of tone-evoked spike trains in auditory cortex and lateral amygdala. Neuron 19, 613-624 (1997).
7. Blair, H.T., Schafe, G.E., Bauer, E.P., Rodrigues, S.M. & LeDoux, J.E. Synaptic plasticity in the lateral amygdala: a cellular hypothesis of fear conditioning. Learn. Mem. 8, 229-242 (2001).
8. LeDoux, J.E. & Gorman, J.M. A call to action: overcoming anxiety through active coping. Am. J. Psychiatry 158, 1953-1955 (2001).
9. Price, J.L. & Amaral, D.G. An autoradiographic study of the projections of the central nucleus of the monkey amygdala. J. Neurosci. 1, 1242-1259 (1981).
10. Davis, M. & Whalen, P.J. The amygdala: vigilance and emotion. Mol. Psychiatry 6, 13-34 (2001).
11. Simon, H., Le Moal, M. & Calas, A. Efferents and afferents of the ventral tegmental-A10 region studied after local injection of [3H]leucine and horseradish peroxidase. Brain Res. 178, 17-40 (1979).
12. Hopkins, D.A. & Holstege, G.G. Amygdaloid projections to the mesencephalon, pons and medulla oblongata in the cat. Exp. Brain Res. 32, 529-547 (1978).
13. Everitt, B.J. & Robbins, T.W. Amygdala-ventral striatal interactions and reward-related processes. In The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction (ed. Aggleton, J.P.) 401-429 (Wiley-Liss, New York, 1992).
14. LaBar, K.S., LeDoux, J.E., Spencer, D.D. & Phelps, E.A. Impaired fear conditioning following unilateral temporal lobectomy in humans. J. Neurosci. 15, 6846-6855 (1995).
15. Bechara, A. et al. Double dissociation of conditioning and declarative knowledge relative to the amygdala and hippocampus in humans. Science 269, 1115-1118 (1995).
16. LaBar, K.S. & Phelps, E.A. Reinstatement of conditioned fear in humans is context dependent and impaired in amnesia. Behav. Neurosci. 119, 677-686 (2005).
17. Ochsner, K.N. & Gross, J.J. The cognitive control of emotion. Trends Cogn. Sci. 9, 242-249 (2005).
18. Robbins, T.W. Chemistry of the mind: neurochemical modulation of prefrontal cortical function. J. Comp. Neurol. 493, 140-146 (2005).
19. Quirk, G.J., Garcia, R. & Gonzalez-Lima, F. Prefrontal mechanisms in extinction of conditioned fear. Biol. Psychiatry 60, 337-343 (2006).
20. Phelps, E.A., Delgado, M.R., Nearing, K.I. & LeDoux, J.E. Extinction learning in humans: role of the amygdala and vmPFC. Neuron 43, 897-905 (2004).
21. Öhman, A. & Soares, J. On the automatic nature of phobic fear: conditioned electrodermal responses to masked fear-relevant stimuli. J. Abnorm. Psychol. 102, 121-132 (1993).
22. Öhman, A. & Mineka, S. Fears, phobias, and preparedness: toward an evolved module of fear and fear learning. Psychol. Rev. 108, 483-522 (2001).
23. Morris, J.S., Öhman, A. & Dolan, R.J. Conscious and unconscious emotional learning in the amygdala. Nature 393, 467-470 (1998).
24. Cook, E.W., Hodes, R.L. & Lang, P.J. Preparedness and phobia: effects of stimulus content on human visceral conditioning. J. Abnorm. Psychol. 95, 195-207 (1986).
25. Olsson, A., Ebert, J.P., Banaji, M.R. & Phelps, E.A. The role of social groups in the persistence of learned fear. Science 309, 785-787 (2005).
26. Hauser, M.D. The Evolution of Communication (MIT Press, Cambridge, Massachusetts, USA, 1996).
27. Thorpe, W.H. Learning and Instinct in Animals (2nd ed.) (Harvard Univ. Press, Cambridge, Massachusetts, USA, 1963).
28. Zajonc, R.B. Social facilitation. Science 149, 269-274 (1965).
29. Galef, B.G. & Laland, K.N. Social learning in animals: empirical studies and theoretical models. BioSci 55, 489-499 (2005).
30. Heyes, C.M. Imitation without perspective-taking. Behav. Brain Sci. 16, 524-525 (1993).
31. Whiten, A., Horner, V. & de Waal, F.B. Conformity to cultural norms of tool use in chimpanzees. Nature 437, 737-740 (2005).
32. Keller, M., Perrin, G., Meurisse, M., Ferreira, G. & Levy, F. Cortical and medial amygdala are both involved in the formation of olfactory offspring memory in sheep. Eur. J. Neurosci. 20, 3433-3441 (2004).
33. Curio, E. Cultural transmission of enemy recognition. In Social Learning: Psychological and Biological Perspectives (eds. Zentall, R.E. & Galef, B.G. Jr.) 75-97 (Erlbaum, Hillsdale, New Jersey, USA, 1988).
34. Kavaliers, M., Choleris, E. & Colwell, D.D. Learning from others to cope with biting flies: social learning of fear-induced conditioned analgesia and active avoidance. Behav. Neurosci. 115, 661-674 (2001).
35. John, E.R., Chesler, P., Bartlett, F. & Victor, I. Observation learning in cats. Science 59, 1489-1491 (1968).
36. Munksgaard, L., DePassille, A.M., Rushen, J., Herskin, M.S. & Kristensen, A.M. Dairy cows' fear of people: social learning, milk yield and behaviour at milking. Appl. Anim. Behav. Sci. 73, 15-26 (2001).
37. Berber, S.M. Conditioning through vicarious instigation. Psychol. Rev. 69, 450-466 (1962).
38. Hygge, S. & Ohman, A. Modeling processes in the acquisition of fears: vicarious electrodermal conditioning to fear-relevant stimuli. J. Pers. Soc. Psychol. 36, 271-279 (1978).
39. Mineka, S. & Cook, M. Mechanisms involved in the observational conditioning of fear. J. Exp. Psychol. Gen. 122, 23-38 (1993).
40. Mineka, S., Davidson, M., Cook, M. & Keir, R. Observational conditioning of snake fear in rhesus monkey. J. Abnorm. Psychol. 93, 355-372 (1984).
41. Olsson, A. & Phelps, E.A. Learned fear of ''unseen'' faces after Pavlovian, observational, and instructed fear. Psychol. Sci. 15, 822-828 (2004).
42. Olsson, A., Nearing, K.I. & Phelps, E.A. Learning fears by observing others: the neural systems of social fear transmission. Soc. Cog. Affect. Neurosci. 2, 3-11 (2007).
43. Vaughan, K.B. & Lanzetta, J.T. Vicarious instigation and conditioning of facial expressive and autonomic responses to a model's expressive display of pain. J. Pers. Soc. Psychol. 38, 909-923 (1980).
44. Ekman, P. Emotion in the Human Face (Cambridge Univ. Press, New York, 1982).
45. Rolls, E.T. The Brain and Emotion (Oxford Univ. Press, New York, 1999).
46. Gerull, F.C. & Rapee, R.M. Mother knows best: effects of maternal modeling on the acquisition of fear and avoidance behavior in toddlers. Behav. Res. Ther. 40, 279-287 (2002).
47. Bandura, A. Social Learning Theory (General Learning Press, New York, 1977).
48. Rachman, S. The conditioning theory of fear acquisition: a critical examination. Behav. Res. Ther. 19, 439-447 (1977).
49. Bandura, A. & Menlove, F.L. Factors determining vicarious extinction of avoidance behavior through symbolic modeling. J. Pers. Soc. Psychol. 8, 99-108 (1968).
50. Mineka, S. & Zinbarg, R. A contemporary learning theory perspective on the etiology of anxiety disorders: it's not what you thought it was. Am. Psychol. 61, 10-26 (2006).
51. Lanzetta, J.T. & Englis, B.G. Expectations of cooperation and competition and their effects on observers' vicarious emotional responses. J. Pers. Soc. Psychol. 56, 543-554 (1989).
52. Singer, T. et al. Empathic neural responses are modulated by the perceived fairness of others. Nature 439, 466-469 (2006).
53. Bennet, G., Galef, J.R. & Durlach, P.J. Absence of blocking, overshadowing, latent inhibition in social enhancement of food preferences. Ann. Learn. Behav. 21, 214-220 (1993).
54. White, D.J. & Galef, B.J. Social influence on avoidance of dangerous stimuli by rats. Ann. Learn. Behav. 26, 433-438 (1998).
55. Lanzetta, J.T. & Orr, S.P. Influence of facial expressions on the classical conditioning of fear. J. Pers. Soc. Psychol. 39, 1081-1087 (1980).
56. Amaral, D.G. The amygdala, social behavior, and danger detection. Ann. NY Acad. Sci. 1000, 337-347 (2003).
57. Ross, R.S. & Eichenbaum, H. Dynamics of hippocampal and cortical activation during consolidation of a nonspatial memory. J. Neurosci. 26, 4852-4859 (2006).
58. Squires, A.S., Peddle, R., Milway, S.J. & Harley, C.W. Cytotoxic lesions of the hippocampus do not impair social recognition memory in socially housed rats. Neurobiol. Learn. Mem. 85, 95-101 (2005).
59. Schneider, M. & Koch, M. Deficient social and play behavior in juvenile and adult rats after neonatal cortical lesion: effects of chronic pubertal cannabinoid treatment. Neuropsychopharmacology 30, 944-957 (2005).
60. Hooker, C.I., Germine, L.T., Knight, R.T. & D'Esposito, M. Amygdala response to facial expressions reflects emotional learning. J. Neurosci. 26, 8915-8922 (2006).
61. Rolls, E.T., Tovée, M.J., Purcell, D.G., Stewart, A.L. & Azzopardi, P. The responses of neurons in the temporal cortex of primates and face identification and detection. Exp. Brain Res. 101, 473-484 (1994).
62. Barton, R.A., Aggleton, J.P. & Grenyer, R. Evolutionary coherence of the mammalian amygdala. Proc. Biol. Sci. 270, 539-543 (2003).
63. Young, M.P., Scannell, J.W., Burns, G.A. & Blakemore, C. Analysis of connectivity: neural systems in the cerebral cortex. Rev. Neurosci. 5, 227-250 (1994).
64. Langford, D.J. et al. Social modulation of pain as evidence for empathy in mice. Science 312, 1967-1970 (2006).
65. Masserman, J.H., Wechkin, S. & Terris, W. "Altruistic" behavior in rhesus monkeys. Am. J. Psychiatry 121, 584-585 (1964).
66. Hauser, M. et al. Give unto others: genetically unrelated cotton-top tamarin monkeys preferentially give food to those who altruistically give food back. Proc. Biol. Sci. 270, 2363-2370 (2003).
67. Gallese, V., Keysers, C. & Rizzolatti, G. A unifying view of the basis of social cognition. Trends Cogn. Sci. 8, 396-403 (2004).
68. Preston, S.D. & de Waal, F.B. Empathy: its ultimate and proximate bases. Behav. Brain Sci. 25, 1-20 (2002).
69. Whalen, P.J. et al. Masked presentations of emotional facial expressions modulate amygdala activity without explicit knowledge. J. Neurosci. 18, 411-418 (1998).
70. Kim, H. et al. Contextual modulation of amygdala responsivity to surprised faces. J. Cogn. Neurosci. 16, 1730-1745 (2004).
71. Peyron, R., Laurent, B. & Garcia-Larrea, L. Functional imaging of brain responses to pain. A review and meta-analysis. Neurophysiol. Clin. 30, 263-288 (2000).
72. Critchley, H.D. Neural mechanisms of autonomic, affective, and cognitive integration. J. Comp. Neurol. 493, 154-166 (2005).
73. Jackson, P.L., Meltzoff, A.N. & Decety, J. How do we perceive the pain of others? A window into the neural processes involved in empathy. Neuroimage 24, 771-779 (2005).
74. Morrison, I., Lloyd, D., di Pellegrino, G. & Roberts, N. Responses to pain in anterior cingulate cortex: is empathy a multisensory issue? Cogn. Affect. Behav. Neurosci. 4, 270-278 (2004).
75. Singer, T. et al. Empathy for pain involves the affective but not sensory components of pain. Science 303, 1157-1162 (2004).
76. Lamm, C., Batson, C.D. & Decety, J. The neural substrate of human empathy: effects of perspective-taking and cognitive appraisal. J. Cogn. Neurosci. 19, 42-58 (2007).
77. Ochsner, K.N. et al. Reflecting upon feelings: an fMRI study of neural systems supporting the attribution of emotion to self and other. J. Cogn. Neurosci. 16, 1746-1772 (2004).
78. Mitchell, J.P., Heatherton, T.F. & Macrae, C.N. Distinct neural systems subserve person and object knowledge. Proc. Natl. Acad. Sci. USA 99, 15238-15243 (2002).
79. Amodio, D.M. & Frith, C.D. Meeting of minds: the medial frontal cortex and social cognition. Nat. Rev. Neurosci. 7, 268-277 (2006).
80. Myers, R.E., Swett, C. & Miller, M. Loss of social group affinity following prefrontal lesions in free-ranging macaques. Brain Res. 64, 257-269 (1973).
81. Beer, J.S., Heerey, E.A., Keltner, D., Scabini, D. & Knight, R.T. The regulatory function of self-conscious emotion: insights from patients with orbitofrontal damage. J. Pers. Soc. Psychol. 85, 594-604 (2003).
82. Ongür, D., Ferry, A.T. & Price, J.L. Architectonic subdivision of the human orbital and medial prefrontal cortex. J. Comp. Neurol. 460, 425-449 (2003).
83. Gilbert, S.J. et al. Functional specialization within rostral prefrontal cortex (area 10): a meta-analysis. J. Cogn. Neurosci. 18, 932-948 (2006).
84. Kosslyn, S.M. & Thompson, W.L. When is early visual cortex activated during visual mental imagery? Psychol. Bull. 129, 723-746 (2003).
85. Tulving, E. Episodicmemory: frommind to brain. Annu. Rev. Psychol. 53, 1-25 (2002).
86. Hassabis, D., Kumaran, D., Vann, S.D. & Maguire, E.A. Patients with hippocampal amnesia cannot imagine new experiences. Proc. Natl. Acad. Sci. USA 104, 1726-1735 (2007).
87. Schacter, D.L. & Addis, D.R. The cognitive neuroscience of constructive memory: remembering the past and imagining the future. Phil. Trans. R. Soc. Lond. B 362, 773-786 (2007).
88. Buckner, R.L. & Carroll, D.C. Self-projection and the brain. Trends Cogn. Sci. 11, 49-57 (2007).
89. King, N.J., Gullone, E. & Ollendick, T.H. Etiology of childhood phobias: current status of Rachman's three pathways theory. Behav. Res. Ther. 36, 297-309 (1998).
90. Field, A.P., Argyris, N.G. & Knowles, K.A. Who's afraid of the big bad wolf: a prospective paradigm to test Rachman's indirect pathways in children. Behav. Res. Ther. 39, 1259-1276 (2001).
91. Grillon, C., Ameli, R., Merikangas, K., Woods, S.W. & Davis, M. Fear-potentiated startle: effects of anticipatory anxiety on the acoustic blink reflex. Psychophysiology 28, 588-595 (1991).
92. Hugdahl, K. & Öhman, A. Effects of instruction acquisition and extinction of electrodermal responses to fear-relevant stimuli. J. Exp. Psychol. [Hum. Learn.] 3, 608-618 (1977).
93. Phelps, E.A. et al. Activation of the amygdala by cognitive representations of fear. Nat. Neurosci. 4, 437-441 (2001).
94. Shi, C. & Davis, M. Pain pathways involved in fear conditioning measured with fearpotentiated startle: lesion studies. J. Neurosci. 19, 420-430 (1999).
95. Gazzaniga, M.S. & LeDoux, J.E. The Integrated Mind (Plenum Press, New York, 1978).
96. Plotkin, H.C. & Odling-Smee, F.J. A multiple level model of evolution and its implications for sociobiology. Behav. Brain Sci. 4, 225-268 (1981).
97. Danchin, E., Giraldeau, L.A., Valone, T.J. &Wagner, R.H. Public information: from nosy neighbors to cultural evolution. Science 305, 487-491 (2004).
98. Büchel, C., Morris, J., Dolan, R.J. & Friston, K.J. Brain systems mediating aversive conditioning: an event-related fMRI study. Neuron 20, 947-957 (1998).
99. LaBar, K.S., Gatenby, J.C., Gore, J.C., LeDoux, J.E. & Phelps, E.A. Human amygdala activation during conditioned fear acquisition and extinction: a mixed-trial fMRI study. Neuron 20, 937-945 (1998).
100. Schultz, W. et al. A neural substrate of prediction and reward. Science 275, 1593-1599 (1997).