The Human Amygdala: An Evolved System for Relevance Detection

Reviews in the Neurosciences

Volumn 14, Issue 4, 2003, Pages 303-316

  Sander, David ^a   Grafman, Jordan ^b   Zalla, Tiziana ^c  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^c INSTITUT DES SCIENCES COGNITIVES   (France)

Author keywords

Appraisal; Emotion; Evolutionary psychology; Human brain; Social cognition; Temporal lobe

Indexed keywords

ACCURACY; AMYGDALOID NUCLEUS; BRAIN DEVELOPMENT; COGNITION; EMOTION; EVOLUTION; FEAR; HUMAN; NERVOUS SYSTEM; NEUROMERE; NONHUMAN; PRIORITY JOURNAL; REVIEW;

EID: 0344013574     PISSN: 03341763     EISSN: None     Source Type: Journal    
DOI: 10.1515/REVNEURO.2003.14.4.303     Document Type: Review

References (112)

1. Aalto S, Naatanen P, Wallius E, Metsahonkala L, Stenman H, Niem PM, Karlsson H. Neuroanatomical substrata of amusement and sadness: a PET activation study using film stimuli. NeuroReport 2002; 13: 67-73.
2. Adolphs R. The neurobiology of social cognition. Curr Opin Neurobiol 2001; 11: 231-239.
3. Adolphs R. Neural systems for recognizing emotion. Curr Opin Neurobiol 2002; 12: 169-177.
4. Adolphs R. Cognitive neuroscience of human social behaviour. Nat Rev Neurosci 2003; 4: 165-178.
5. Adolphs R, Tranel D. Intact recognition of emotional prosody following amygdala damage. Neuropsychologia 1999; 37: 1285-1292.
6. Adolphs R, Tranel D. Emotion recognition and the human amygdala. In: Aggleton JP, ed. The Amygdala: A Functional Analysis. Oxford: Oxford University Press, 2000; 587-630.
7. Adolphs R, Tranel D, Damasio AR. The human amygdala in social judgment. Nature 1998; 393: 470-474.
8. Adolphs R, Tranel D, Damasio H, Damasio A. Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala. Nature 1994; 372: 669-672.
9. Adolphs R, Tranel D, Damasio H, Damasio AR. Fear and the human amygdala. J Neurosci 1995; 15: 5879-5891.
10. Aggleton JP. The Amygdala: Neurobiological Aspects of Emotion, Memory and Mental Dysfunction. New York: Wiley-Liss, 1992.
11. nd Ed. Oxford: Oxford University Press, 2000.
12. Amaral DG, Price JL, Pitkänen A, Carmichael ST. Anatomical organization of the primate amygdaloid complex. In: Aggleton JP, ed. The Amygdala: Neurobiological Aspects of Emotion, Memory and Mental Dysfunction. New York: Wiley-Liss, 1992; 1-66.
13. Amaral DG. The primate amygdala and the neurobiology of social behavior: implications for understanding social anxiety. Biol Psychiatry 2002; 51: 11-17.
14. Anderson AK, Phelps EA. Intact recognition of vocal expressions of fear following bilateral lesions of the human amygdala. NeuroReport 1998; 9: 3607-3613.
15. Baron-Cohen S, Ring HA, Wheelwright S, Bullmore ET, Brammer MJ, Simmons A, Williams SCR. Social intelligence in the normal and autistic brain: an fMRI study. Eur J Neurosci 1999; 11: 1891-1898.
16. Barton RA, Aggleton JP. Primate evolution and the amygdala. In: Aggleton JP, ed. The Amygdala: A Functional Analysis. Oxford: Oxford University Press, 2000; 479-508.
17. Barton RA, Aggleton JP, Grenyer R. Evolutionary coherence of the mammalian amygdala. Proc R Soc Lond B Biol Sci 2003; 270: 539-543.
18. Baxter MG, Murray EA. The amygdala and reward. Nat Rev Neurosci 2002; 3: 563-573.
19. Beauregard M, Lévesque J, Bourgouin P. Neural correlates of conscious self-regulation of emotion. J Neurosci 2001; 21: RC165 (1-6).
20. Bechara A, Damasio H, Damasio AR, Lee GP. Different contributions of the human amygdala and ventromedial prefrontal cortex to decision-making. J Neurosci 1999; 19: 5473-5481.
21. Bechara A, Tranel D, Damasio H, Adolphs R, Rockland C, Damasio AR. Double dissociation of conditioning and declarative knowledge relative to the amygdala and hippocampus in humans. Science 1995; 269: 1115-1118.
22. Blair RJR, Morris JS, Frith CD, Perret DI, Dolan RJ. Dissociable neural responses to facial expressions of sadness and anger. Brain 1999; 122: 883-893.
23. Bonda E, Petrides M, Ostry D, Evans A. Specific involvement of human parietal systems and the amygdala in the perception of biological motion. J Neurosci 1996; 16: 3737-3744.
24. Breiter HC, Etcoff NL, Whalen PJ, Kennedy WA, Rauch SL, Buckner RL, Strauss MM, Hyman SE, Rosen BR. Response and habituation of the human amygdala during visual processing of facial expression. Neuron 1996; 17: 875-887.
25. Broks P, Young AW, Maratos EJ, Coffey PJ, Calder AJ, Isaac C, Mayes AR, Hodges JR, Montaldi D, Cezayirli E, Roberts N, Hadley D. Face processing impairments after encephalitis: amygdala damage and recognition of fear. Neuropsychologia 1998; 36: 59-70.
26. Büchel C, Dolan RJ. Classical fear conditioning in functional neuroimaging. Curr Opin Neurobiol 2000; 10: 219-223.
27. Calder AJ, Lawrence AD, Young AW. Neuropsychology of fear and loathing. Nat Rev Neurosci 2001; 2: 352-363.
28. Calder AJ, Young AW, Rowland D, Perrett DI, Hodges JR, Etcoff NL. Facial emotion recognition after bilateral amygdala damage: differentially severe impairment of fear. Cogn Neuropsychol 1996; 13: 699-745.
29. Canli T, Sivers H, Whitfield SL, Gotlib IH, Gabrieli JDE. Amygdala response to happy faces as a function of extraversion. Science 2002; 296: 2191.
30. Canli T, Zhao Z, Desmond JE, Kang E, Gross J, Gabrieli JDE. An fMRI study of personality influences on brain reactivity to emotional stimuli. Behav Neurosci 2001; 115: 33-42.
31. Carmel D, Bentin S. Domain specificity and expertise: factors influencing distinct processing of faces. Cognition 2002; 83: 1-29.
32. Cheng DT, Knight DC, Smith CN, Stein EA, Helmstetter FJ. Functional MRI of human amygdala activity during Pavlovian fear conditioning: stimulus processing versus response expression. Behav Neurosci 2003; 117: 3-10.
33. Cosmides L, Tooby J. Origins of domain specificity: the evolution of functional organization. In: Hirschfeld LA, Gelman SA, eds. Mapping the Mind. Domain Specificity in Cognition and Culture. Cambridge: Cambridge University Press, 1994; 85-116.
34. Davis M, Whalen PJ. The amygdala: vigilance and emotion. Mol Psychiatry 2001; 6: 13-34.
35. de Gelder B, Vroomen J, Pourtois G, Weiskrantz L. Non-conscious recognition of affect in the absence of the striate cortex. NeuroReport 1999; 10: 3759-3763.
36. de Gelder B, Pourtois G, Weiskrantz L. Fear recognition in the voice is modulated by unconsciously recognized facial expressions but not by unconsciously recognized affective pictures. Proc Natl Acad Sci USA 2002; 99: 4121-4126.
37. Dolan RJ, Morris JS, de Gelder B. Crossmodal binding of fear in voice and face. Proc Natl Acad Sci USA 2001; 98: 10006-10010.
38. Dubois S, Rossion B, Schiltz C, Bodart JM, Michel C, Bruyer R, Crommelinck M. Effect of familiarity on the processing of human faces. Neuroimage 1999; 9: 278-289.
39. Duchaine B, Cosmides L, Tooby J. Evolutionary psychology and the brain. Curr Opin Neurobiol 2001; 11: 225-230.
40. Dumont EC, Martina M, Samson RD, Drolet G, Paré D. Physiological properties of central amygdala neurons: species differences. Eur J Neurosci 2002; 15: 545-552.
41. Ekman P. Basic emotions. In: Dalgleish T, Power M, eds. Handbook of Cognition and Emotion. Chichester: John Wiley & Sons, Ltd., 1999.
42. Fine C, Blair RJR. The cognitive and emotional effects of amygdala damage. NeuroReport 2000; 6: 435-450.
43. Garavan H, Pendergrass JC, Ross TJ, Stein EA, Risinger RC. Amygdala response to both positively and negatively valenced stimuli. NeuroReport 2001; 12: 2779-2783.
44. George N, Driver J, Dolan RJ. Seen gaze-direction modulates fusiform activity and its coupling with other brain areas during face processing. Neuroimage 2001; 13: 1102-1112.
45. Gorno-Tempini ML, Pradelli S, Serafini M, Pagnoni G, Baraldi P, Porro C, Nicoletti R, Umita C, Nichelli P. Explicit and incidental facial expression processing: an fMRI study. Neuroimage 2001; 14: 465-473.
46. Hamann S. Cognitive and neural mechanisms of emotional memory. Trends Cogn Sci 2001; 5: 394-400.
47. Hamann SB, Ely TD, Grafton ST, Kilts CD. Amygdala activity related to enhanced memory for pleasant and aversive stimuli. Nat Neurosci 1999; 2: 289-293.
48. Hamann SB, Ely TD, Hoffman JM, Kilts CD. Ecstasy and agony: activation of the human amygdala in positive and negative emotion. Psychol Sci 2002; 13: 135-141.
49. Hamann S, Mao H. Positive and negative emotional verbal stimuli elicit activity in the left amygdala. NeuroReport 2002; 13: 15-19.
50. Hart AJ, Whalen PJ, Shin LM, McInerney SC, Fischer H, Rauch SL. Differential response in the human amygdala to racial outgroup vs ingroup face stimuli. NeuroReport 2000; 11: 2351-2355.
51. Holland PC, Gallagher M. Amygdala circuitry in attentional and representational processes. Trends Cogn Sci 1999; 3: 65-73.
52. Irwin W, Davidson RJ, Lowe MJ, Mock BJ, Sorenson JA, Turski PA. Human amygdala activation detected with echo-planar functional magnetic resonance imaging. NeuroReport 1996; 7: 1765-1769.
53. Jones EG, Burton H. A projection from the medial pulvinar to the amygdala in primates. Brain Res 1976; 104: 142-147.
54. Kahn I, Yeshurun Y, Rotshtein P, Fried I, Ben-Bashat D, Hendler T. The role of the amygdala in signaling prospective outcome of choice. Neuron 2002; 33: 983-994.
55. Karama S, Lecours AR, Leroux J-M, Bourgouin P, Beaudoin G, Joubert S, Beauregard M. Areas of brain activation in males and females during viewing of erotic film excerpts. Hum Brain Mapp 2002; 16: 1-13.
56. Kawashima R, Sugiura M, Kato T, Nakamura A, Hatano K, Ito K, Fukuda H, Kojima S, Nakamura K. The human amygdala plays an important role in gaze monitoring. A PET study. Brain 1999; 122: 779-783.
57. Kjelstrup KG, Tuvnes FA, Steffenach HA, Murison R, Moser EI, Moser M-B. Reduced fear expression after lesions of the ventral hippocampus. Proc Natl Acad Sci USA 2002; 99: 10825-10830.
58. Klüver H, Bucy PC. An analysis of functions of the temporal lobes in monkeys, with special reference to «psychic blindness». J Psychol 1938; 5: 33-54.
59. Kosaka H, Omori M, Murata T, Iidaka T, Yamada H, Okada T, Takahashi T, Sadato N, Itoh H, Yonekura Y, Wada Y. Differential amygdala response during facial recognition in patients with schizophrenia: an fMRI study. Schizophr Res 2002; 7: 87-95.
60. LaBar KS, Gitelman DR, Parrish TB, Kim Y-H, Nobre A, Mesulam M-M. Hunger selectivity modulates corticolimbic activation to food stimuli in humans. Behav Neurosci 2001; 115: 493-500.
61. LeDoux JE. The Emotional Brain. London: Weidenfeld & Nicolson, 1996.
62. Levesque J, Eugene F, Joanette Y, Paquette V, Mensour B, Beaudoin G, Leroux JM, Bourgouin P, Beauregard M. Neural circuitry underlying voluntary suppression of sadness. Biol Psychiatry 2003; 53: 502-510.
63. McGaugh JL. Memory consolidation and the amygdala: a systems perspective. Trends Neurosci 2002; 25: 456-461.
64. Meunier M, Bachevalier J, Murray EA, Malkova L, Mishkin M. Effects of aspiration versus neurotoxic lesions of the amygdala on emotional responses in rhesus monkeys. Eur J Neurosci 1999; 11: 4403-4418.
65. Morris JS, Büchel C, Dolan RJ. Parallel neural responses in amygdala subregions and sensory cortex during implicit fear conditioning. Neuroimage 2001; 13: 1044-1052.
66. Morris JS, Dolan RJ. Involvement of human amygdala and orbitofrontal cortex in hunger-enhanced memory for food stimuli. J Neurosci 2001; 21: 5304-5310.
67. Morris JS, de Gelder B, Weiskrantz L, Dolan RJ. Differential extrageniculostriate and amygdala responses to presentation of emotional faces in a cortically blind field. Brain 2001; 124: 1241-1252.
68. Morris JS, Frith CD, Perret DI, Rowland D, Young AW, Calder AJ, Dolan RJ. A differential neural response in the human amygdalia to fearful and happy facial expressions. Nature 1996; 383: 812-815.
69. Morris JS, Öhman A, Dolan RJ. Conscious and unconscious emotional learning in the amygdala. Nature 1998; 393: 467-470.
70. Morris JS, Öhman A, Dolan RJ. A subcortical pathway to the right amygdala mediating «unseen» fear. Proc Natl Acad Sci USA 1999; 96: 1680-1685.
71. O'Doherty JP, Deichmann R, Critchley HD, Dolan RJ. Neural responses during anticipation of a primary taste reward. Neuron 2002; 33: 815-826.
72. O'Doherty J, Rolls ET, Francis S, Bowtell R, McGlone F. Representation of pleasant and aversive taste in the human brain. J Neurophysiol 2001; 85: 1315-1321.
73. Öhman A. Automaticity and the amygdala: nonconscious responses to emotional faces. Curr Directions Psychol Sci 2002; 11: 62-66.
74. Öhman A, Mineka S. Fears, phobias, and preparedness: toward an evolved module of fear and fear learning. Psychol Rev 2001; 108: 483-522.
75. Paradiso S, Johnson DL, Andreasen NC, O'Leary DS, Watkins GL, Boles Ponto LL, Hichwa RD. Cerebral blood flow changes associated with attribution of emotional valence to pleasant, unpleasant, and neutral visual stimuli in a PET study of normal subjects. Am J Psychiatry 1999; 156: 1618-1629.
76. Paré D, Collins DR, Pelletier JG. Amygdala oscillations and the consolidation of emotional memories. Trends Cogn Sci 2002; 6: 306-314.
77. Pessoa L, McKenna M, Gutierrez E, Ungerleider LG. Neural processing of emotional faces requires attention. Proc Natl Acad Sci USA 2002; 99: 11458-11463.
78. Phan KL, Taylor SF, Welsh RC, Decker LR, Noll DC, Nichols TE, Britton JC, Liberzon I. Activation of the medial prefrontal cortex and extended amygdala by individual ratings of emotional arousal: a fMRI study. Biol Psychiatry 2003; 53: 211-215.
79. Phelps EA, O'Connor KJ, Cunningham WA, Sumie Funayama E, Gatenby JC, Gore JC, Banaji MR. Performance on indirect measures of race evaluation predicts amygdala activation. J Cogn Neurosci 2000; 12: 729-738.
80. Phelps EA, O'Connor KJ, Gatenby JC, Gore JC, Grillon C, Davis M. Activation of the left amygdala to a cognitive representation of fear. Nat Neurosci 2001; 4: 437-441.
81. Phillips ML, Medford N, Young AW, Williams L, Williams SCR, Bullmore ET, Gray JA, Brammer MJ. Time courses of left and right amygdalar responses to fearful facial expressions. Hum Brain Mapp 2001; 12: 193-202.
82. Phillips ML, Young AW, Scott SK, Calder AJ, Andrew C, Giampietro V, Williams SCR, Bullmore ET, Brammer M, Gray JA. Neural responses to facial and vocal expressions of fear and disgust. Proc R Soc Lond B Biol Sci 1998; 265: 1809-1817.
83. Phillips ML, Young AW, Senior C, Brammer M, Andrew C, Calder AJ, Bullmore ET, Perett DI, Rowland D, Williams SCR, Gray JA, David AS. A specific neural substrate for perceiving facial expressions of disgust. Nature 1997; 389: 495-498.
84. Portas CM, Krakow K, Allen P, Josephs O, Armony JL, Frith CD. Auditory processing across the sleep-wake cycle: simultaneous EEG and fMRI monitoring in humans. Neuron 2000; 28: 991-999.
85. Rapcsak SZ, Galper SR, Comer JF, Reminger SL, Nielsen L, Kaszniak AW, Verfaellie M, Laguna JF, Labiner DM, Cohen RA. Fear recognition deficits after focal brain damage. Neurology 2000; 54: 575-581.
86. Redouté J, Stoléru S, Grégoire M-C, Costes N, Cinotti L, Lavenne F, Le Bars D, Forest MG, Pujol JF. Brain processing of visual sexual stimuli in human males. Hum Brain Mapp 2000; 1I: 162-177.
87. Royet J-P, Zald D, Versace R, Costes N, Lavenne F, Koenig O, Gervais R. Emotional responses to pleasant and unpleasant olfactory, visual, and auditory stimuli: a positron emission tomography study. J Neurosci 2000; 20: 7752-7759.
88. Sander D, Koenig O. No inferiority complex in the study of emotion complexity: a cognitive neuroscience computational architecture of emotion. Cogn Sci Q 2002; 2: 249-272.
89. Scherer KR, Schorr A, Johnstone T. Appraisal Processes in Emotion: Theory, Methods, Research. New York: Oxford University Press, 2001.
90. Schienle A, Stark R, Walter B, Blecker C, Ott U, Kirsch P, Sammer G, Vaitl D. The insula is not specifically involved in disgust processing: an fMRI study. NeuroReport 2002; 13: 2023-2026.
91. Schneider F, Habel U, Kessler C, Salloum JB, Posse S. Gender differences in regional cerebral activity during sadness. Hum Brain Mapp 2000; 9: 226-238.
92. Schwartz S, Maquet P, Frith C. Neural correlates of perceptual learning: a functional MRI study of visual texture discrimination. Proc Natl Acad Sci USA 2002; 99: 17137-17142.
93. Scott SK, Young AW, Calder AJ, Hellawell DJ, Aggleton JP, Johnson M. Impaired auditory recognition of fear and anger following bilateral amygdala lesions. Nature 1997; 385: 254-257.
94. Siegle GJ, Steinhauer SR, Thase ME, Stenger VA, Carter CS. Can't shake that feeling: event-related fMRI assessment of sustained amygdala activity in response to emotional information in depressed individuals. Biol Psychiatry 2002; 51: 693-707.
95. Small DM. Toward an understanding of the brain substrates of reward in humans. Neuron 2002; 33: 668-671.
96. Sprengelmeyer R, Young AW, Schroeder U, Grossenbacher PG, Federlein J, Bïttner T, Przuntek H. Knowing no fear. Proc R Soc Lond B Biol Sci 1999; 266: 2451-2456.
97. Swanson LW, Petrovich GD. What is the amygdala? Trends Neurosci 1998; 21: 323-331.
98. Vuilleumier P, Armony JL, Driver J, Dolan, RJ. Effects of attention and emotion on face processing in the human brain: an event-related fMRI study. Neuron 2001; 3: 829-841.
99. Weiskrantz L. Behavioral changes associated with ablation of the amygdaloid complex in monkeys. J Comp Psychol 1956; 49: 381-391.
100. Whalen PJ. Fear, vigilance and ambiguity: initial neuroimaging studies of the human amygdala. Curr Directions Psychol Sci 1998; 7: 177-187.
101. Whalen PJ, Rauch LS, Etcoff NL, McInerney SC, Lee MB, Jenike MA. Masked presentations of emotional facial expressions modulate amygdala activity without explicit knowledge. J Neurosci 1998; 18: 411-418.
102. Whalen PJ, Shin LM, McInerney SC, Fischer H, Wright CI, Rauch SL. A functional MRI study of human amygdala responses to facial expressions of fear versus anger. Emotion 2001; 1: 70-83.
103. Wicker B, Perrett DI, Baron-Cohen S, Decety J. Being the target of another's emotion: a PET study. Neuropsychologia 2003; 41: 139-146.
104. Winston JS, Strange BA, O'Doherty J, Dolan RJ. Automatic and intentional brain responses during evaluation of trustworthiness of faces. Nat Neurosci 2002; 5: 277-283.
105. Wright CI, Fischer H, Whalen PJ, McInerney SC, Shin LM, Rauch SL. Differential prefrontal cortex and amygdala habituation to repeatedly presented emotional stimuli. NeuroReport 2001; 12: 379-383.
106. Wright CI, Martis B, Shin LM, Fischer H, Rauch SL. Enhanced amygdala responses to emotional versus neutral schematic facial expressions. NeuroReport 2002; 13: 785-790.
107. Yang TT, Menon V, Eliez S, Blasey C, White CD, Reid AJ, Gotlib IH, Reiss AL. Amygdalar activation associated with positive and negative facial expressions. NeuroReport 2002; 13: 1737-1741.
108. Young AW, Aggleton JP, Hellawell DJ, Johnson M, Broks P, Hanley JR. Face processing impairments after amygdalectomy. Brain 1995; 118: 15-24.
109. Young MP, Scannel JW, Burns GAPC, Blakemore C. Analysis of connectivity: neural systems in the cerebral cortex. Rev Neurosci 1994; 5: 227-249.
110. Zald D, Pardo JV. Emotion, olfaction, and the human amygdalia: amygdala activation during aversive olfactory stimulation. Proc Natl Acad Sci USA 1997; 94: 4119-4124.
111. Zald D, Lee JT, Fluegel KW, Pardo JV. Aversive gustatory stimulation activates limbic structures in humans. Brain 1998; 121: 1143-1154.
112. Zalla T, Koechlin E, Pietrini P, Basso G, Aquino P, Sirigu A, Grafman J. Differential amygdala responses to winning and losing: a functional magnetic resonance imaging study in humans. Eur J Neurosci 2000; 12: 1764-1770.