Response and habituation of the human amygdala during visual processing of facial expression

Neuron

Volumn 17, Issue 5, 1996, Pages 875-887

  Breiter, Hans C ^a,b   Etcoff, Nancy L ^b   Whalen, Paul J ^b   Kennedy, William A ^a   Rauch, Scott L ^a,b   Buckner, Randy L ^a   Strauss, Monica M ^b   Hyman, Steven E ^b,c   Rosen, Bruce R ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; AMYGDALOID NUCLEUS; ARTICLE; EMOTION; FACE; FACIAL EXPRESSION; FEAR; HABITUATION; HUMAN; HUMAN EXPERIMENT; MALE; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; VISION; VISUAL STIMULATION;

EID: 0030293727     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0896-6273(00)80219-6     Document Type: Article

References (71)

1. Adolphs, R., Tranel, D., Damasio, H., and Damasio, A. (1994). Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala. Nature 372, 669-672.
2. Adolphs, R., Tranel, D., Damasio, H., and Damasio, A.R. (1995). Fear and the human amygdala. J. Neurosci. 15, 5879-5891.
3. Aggleton, J.P., Burton, M.J., and Passingham, R.E. (1980). Cortical and subcortical afferents to the amygdala in the rhesus monkey (Macaca mulatta). Brain Res. 190, 347-368.
4. Amaral, D.G., and Price, J.L. (1984). Amygdalo-cortical projections in the monkey (Macaca fascicularis). J. Comp. Neurol. 230, 465-496.
5. Andreasen, N.C., O'Leary, D.S., Arndt, S., Cizadlo, T., Hurtig, R., Rezai, K., Watkins, G.L., Ponto, L.B., and Hichwa, R.D. (1996). Neural substrates of facial recognition. J. Neuropsych. 8, 139-146.
6. Bandettini, P.A., Wong, E.C., Hinks, R.S., Tikofsky, R.S., and Hyde, J.S. (1992). Time course EPI of human brain function during task activation. Magn. Reson. Med. 25, 390-397.
7. Bechara, A., Tranel, D., Damasio, H., Adolphs, R., Rockland, C., and Damasio, A.R. (1995). Double dissociation of conditioning and declarative knowledge relative to the amygdala and hippocampus in humans. Science 269, 1115-1118.
8. Benkelfat, C., Bradwejn, J., Meyer, E., Ellenbogen, M., Milot, S., Gjedde, A., and Evans, A. (1995). Functional neuroanatomy of CCK4-induced anxiety in normal healthy volunteers. Am. J. Psych. 152, 1180-1191.
9. Bordi, F., and LeDoux, J. (1992). Sensory tuning beyond the sensory system: an initial analysis of auditory response properties of neurons in the lateral amygdaloid nucleus and overlying areas of the striatum. J. Neurosci. 12, 2493-2503.
10. Bordi, F., LeDoux, J., Clugnet, M.C., and Pavlides, C. (1993). Single-unit activity in the lateral nucleus of the amygdala and overlying areas of the striatum in freely behaving rats: rates, discharge patterns, and responses to acoustic stimuli. Behav. Neurosci. 107, 757-769.
11. Breiter, H.C., and Rauch S.L. (1996). Functional MRI and the study of OCD: from symptom provocation to cognitive-behavioral probes of cortico-striatal systems and the amygdala. Neurolmage, in press.
12. Breiter, H.C., Rauch, S.L., Kwong, K.K., Baker, J.R., Weisskoff, R.M., Kennedy, D.N., Kendrick, A.D., Davis, T.L., Jiang, A., Cohen, M.S., Stern, C.E., Belliveau, J.W., Baer, L., O'Sullivan, R.M., Savage, C.R., Jenike, M.A., and Rosen, B.R. (1996). Functional magnetic resonance imaging of symptom provocation in obsessive-compulsive disorder. Arch. Gen. Psych. 53, 595-606.
13. Buckner, R.L., Petersen, S.E., Ojemann, J.G., Miezin, F.M., Squire, L.R., and Raichle, M.E. (1995). Functional anatomical studies of explicit and implicit memory retrieval tasks. J. Neurosci. 15, 12-29.
14. Cador, M., Robbins, T.W., and Everitt, B.J. (1989). Involvement of the amygdala in stimulus-reward associations: interaction with the ventral striatum. J. Neurosci. 30, 77-86.
15. Cahill, L., Haier, R.J., Fallon, J., Alkire, M.T., Tang, C., Keator, D., Wu, J., and McGaugh, J.L. (1996). Amygdala activity at encoding correlated with long-term, free recall of emotional information. Proc. Natl. Acad. Sci. USA 93, 8016-8021.
16. Calder, A.J., Young, A.W., Rowland, D., Perrett, D.I., Hodges, J.R., and Etcoff, N.L. (1996). Facial emotion recognition after bilateral amygdala damage: differentially severe impairment of fear. Cogn. Neuropsych. 13, 699-745.
17. Cohen, M.S., Kosslyn, S.M., Breiter, H.C., DiGirolamo, G.J., Thompson, W.L., Anderson, A.K., Bookheimer, S.Y., Rosen, B.R., and Belliveau, J.W. (1996). Changes in cortical activity during mental rotation: a mapping study using functional MRI. Brain 119, 89-100.
18. Darwin, C. (1872). The Expression of the Emotions in Man and Animals (London: John Murray).
19. Davis, M. (1992). The role of the amygdala in conditioned fear. In The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction, J.P. Aggleton, ed. (New York: Wiley-Liss), pp. 255-306.
20. Drevets, W.C., Videen, T.O., Price, J.L., Preskorn, S.H., Carmichael, S.T., and Raichle, M.E. (1992). A functional anatomical study of unipolar depression. J. Neurosci. 12, 3628-3641.
21. Ekman, P. (1989). The argument and evidence about universals in facial expression of emotion. In Handbook of Social Psychophysiology, H. Wagner and A. Manstead, eds. (New York: Wiley and Sons), pp. 143-164.
22. Ekman, P., and Friesen, W.V. (1976). Pictures of Facial Affect (Palo Alto, California: Consulting Psychologists Press).
23. Ekman, P., Sorenson, E.R., and Friesen, W.V. (1969). Pan-cultural elements in facial displays of emotion. Science 164, 86-88.
24. Everitt, B.J., Morris, K.A., O'Brien, A., and Robbins, T.W. (1991). The basolateral amygdala-ventral striatal system and conditioned place preference: further evidence of limbic-striatal interactions underlying reward-related processes. J. Neurosci. 42, 1-18.
25. Feinberg, T.E., Rifkin, A., Schaffer, C., and Walker, E. (1986). Facial discrimination and emotional recognition in schizophrenia and affective disorders. Arch. Gen. Psych. 43, 276-279.
26. Filipek, P., Richelme, C., Kennedy, D., and Caviness, V. (1994) The young adult human brain: an MRI-based morphometric analysis. Cerebral Cortex 4, 344-360.
27. Fromm, D., and Schopflocher, D. (1984). Neuropsychological test performance in depressed patients before and after drug therapy. Biol. Psych. 19, 55-71.
28. Gaffan, D., and Harrison, S. (1987). Amygdalectomy and disconnection in visual learning for auditory secondary reinforcement by monkeys. J. Neurosci. 7, 2285-2292.
29. Gaffan, D., and Harrison, S. (1988). Disconnection of the amygdala from visual association cortex impairs visual reward-association learning in monkeys. J. Neurosci. 8, 3144-3150.
30. Gallagher, M., and Holland, P.C. (1994). The amygdala complex: multiple roles in associative learning and attention. Proc. Natl. Acad. Sci. USA 97, 11771-11776.
31. George, M.S., Ketter, T.A., Gill, D.S., Haxby, J.V., Ungerleider, L.G., Herscovitch, P., and Post, R.M. (1993). Brain regions involved in recognizing facial emotion or identity: an oxygen-15 PET study. J. Neuropsych. 5, 384-394.
32. Greden, J.F., Genero, N., Price, L., Feinberg, M., and Levine, S. (1986). Facial electromyography in depression. Arch. Gen. Psych. 43, 269-274.
33. Gur, R.C., Erwin, R.J., Gur, R.E., Zwil, A.S., Heimberg, C., and Kraemer, H.C. (1992). Facial emotion discrimination. II. Behavioral findings in depression. Psych. Res. 42, 241-251.
34. Halgren, E., Baudena, P., Heit, G., Clarke, J.M., and Marinkovic, K. (1994). Spatio-temporal stages in face and word processing. II. Depth-recorded potentials in the human frontal and Rolandic cortices. J. Physiol. 88, 1-50.
35. Hamann, S.B., Stefanacci, L., Squire, L.R., Adolphs, R., Tranel, D., Damasio, H., and Damasio, A. (1996). Recognizing facial emotion. Nature 379, 497.
36. Hasselmo, M.E., Rolls, E.T., and Baylis, G.C. (1989). The role of expression and identity in the face-selective responses of neurons in the temporal visual cortex of the monkey. Behav. Brain Res. 32, 203-218.
37. Hatfield, T., Han, J.-S., Conley, M., Gallagher, M., and Holland, P. (1996). Neurotoxic lesions of basolateral, but not central, amygdala interfere with pavlovian second-order conditioning and reinforcer devaluation effects. J. Neurosci. 16, 5256-5265.
38. Haxby, J.V., Horwitz, B., Ungerleider, L.G., Maisog, J.M., Pietrini, P., and Grady, C.L. (1994). The functional organization of human extrastriate cortex: a PET-rCBF study of selective attention to faces and locations. J. Neurosci. 14, 6336-6353.
39. Irwin, W., Davidson, R.J., Lowe, M.J., Mock, B.J., Sorenson, J.A., and Turski, P.A. (1996). Human amygdala activation detected with echo-planar functional magnetic resonance imaging. Neuroreport, in press.
40. Jaeger, J., Borod, J.C., and Peselow, E. (1986). Facial expression of positive and negative emotions in patients with unipolar depression. J. Affect. Disord. 11, 43-50.
41. Jiang, A., Kennedy, D.N., Baker, J.R., Weisskoff, R.M., Tootell, R.B.H., Woods, R.P., Benson, R.R., Kwong, K.K., Brady, T.J., Rosen, B.R., and Belliveau, J.W. (1995). Motion detection and correction in functional MR imaging. Hum. Brain Mapp. 3, 1-12.
42. Jones, B., and Mishkin, M. (1972). Limbic lesion and the problem of stimulus-reinforcement association. Expl. Neurol. 36, 362-377.
43. Kanwisher, N., Chun, M., McDermott, J., and Ledden, P. (1996). Functional imaging of human visual recognition. Cogn. Brain Res., in press.
44. Kapp, B.S., Whalen, P.J., Supple, W.F., and Pascoe, J.P. (1992). Amygdaloid contributions to conditioned arousal and sensory information processing. In The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction, J.P. Aggleton, ed. (New York: Wiley-Liss), pp. 229-254.
45. Kwong, K.K., Belliveau, J.W., Chesler, D.A., Goldberg, I.E., Weiskoff, R.M., Poncelet, B.P., Kennedy, D.N., Hoppel, B.E., Cohen, M.S., Turner, R., Cheng, H.M., Brady, T.J., and Rosen, B.R. (1992). Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation. Proc. Natl. Acad. Sci. USA 89, 5675-5679.
46. LaBar, K.S., LeDoux, J.E., Spencer, D.D., and Phelps, E.A. (1995). Impaired fear conditioning following unilateral temporal lobectomy in humans. J. Neurosci. 15, 6846-6855.
47. LeDoux, J.E. (1992). Emotion and the amygdala. In The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction, J.P. Aggleton, ed. (New York: Wiley-Liss), pp. 339-351.
48. LeDoux, J.E. (1993). Emotional memory: in search of systems and synapses. Ann. NY Acad. Sci. 702, 149-157.
49. Leonard, C.M., Rolls, E.T., Wilson, F.A., and Baylis, G.C. (1985). Neurons in the amygdala of the monkey with responses selective for faces. Behav. Brain Res. 15, 159-176.
50. Mikhailova, E.S., Vladimirova, T.V., Iznak, A.F., Tsusulkovskaya, E.J., and Sushko, N.V. (1996). Abnormal recognition of facial expression of emotions in depressed patients with major depression disorder and schizotypal personality disorder. Biol. Psych. 40, 697-705.
51. Nakamura, K., Mikami, A., and Kubota, K. (1992). Activity of single neurons in the monkey amygdala during performance of a visual discrimination task. J. Neurophysiol. 67, 1447-1463.
52. Ogawa, S., Tank, D.W., Menon, R., Ellermann, J.M., Kim, S.G., Merkle, H., and Ugurbil, K. (1992). Intrinsic signal changes accompanying sensory stimulation: functional brain mapping using MRI. Proc. Natl. Acad. Sci. USA 89, 5951-5955.
53. Perrett, D.I., and Rolls, E.T. (1982). Neural mechanisms underlying the visual analysis of faces. In Advances in Vertebrate Neuroethology, J.-P. Evert, R.R. Capranica, and D.J. Ingle, eds. (New York: Plenum Press).
54. Perrett, D.I., Rolls, E.T., and Caan, W. (1982). Visual neurons responsive to faces in the monkey temporal cortex. Exp. Brain Res. 47, 329-342.
55. Puce, A., Allison, T., Asgari, M., Gore, J.C., and McCarthy, G. (1996). Differential sensitivity of human visual cortex to faces, letterstrings, and textures: a functional magnetic resonance imaging study. J. Neurosci. 16, 5205-5215.
56. Rauch, S.L., van der Kolk, B.A., Fisler, R.E., Alpert, N.M., Orr, S.P., Savage, C.R., Fischman, A.J., Jenike, M.A., and Pitman, R.K. (1996). A symptom provocation study of posttraumatic stress disorder using positron emission tomography and script-driven imagery. Arch. Gen. Psych. 53, 380-387.
57. Reese, T.G., Davis, T.L., and Weisskoff, R.M. (1995). Automated shimming at 1.5T using echo planar image frequency maps. J. Magn. Reson. Imaging 5, 739-745.
58. Rolls, E.T. (1981). Responses of amygdaloid neurons in the primate. In The Amygdaloid Complex, Y. Ben-Ari, ed. (Amsterdam: Elsevier), pp. 383-393.
59. Rolls, E.T. (1984). Neurons in the cortex of the temporal lobe and in the amygdala of the monkey with responses selective for faces. Hum. Neurobiol. 3, 209-222.
60. Rolls, E.T. (1985). Connections, functions and dysfunctions of limbic structures, the prefrontal cortex, and hypothalamus. In The Scientific Basis of Clinical Neurology, M. Swash and C. Kennard, eds. (London: Churchill Livingstone), pp. 201-213.
61. Rolls, E.T. (1991). The processing of face information in the primate temporal lobe. In Processing Images of Faces, V. Bruce and M. Burton, eds. (Norwood, New Jersey: Ablex).
62. Rubinov, D.R., and Post, R.M. (1992). Impaired recognition of affect in facial expression in depressed patients. Biol. Psych. 31, 947-953.
63. Schneider, F., Koch, J.-D., Mattes, R., and Heimann, (1992). Das erkennen von emotionen aus dem gesichtausdruck die viseullen halbfelddarbietungen durch schizophrene und depressive patienten. Nervenearzt 63, 545-550.
64. Schneider, F., Gur, R.E., Alavi, A., Seligman, M.E.P., Mozley, L.H., Smith, R.J., Mozley, P.D., and Gur, R. (1996). Cerebral blood flow changes in limbic regions induced by unsolvable anagram tasks. Am. J. Psych. 153, 206-212.
65. Sergent, J., Ohta, S., MacDonald, B., and Zuck, E. (1994). Segregated processing of facial identity and emotion in the human brain: a PET study. Vis. Cogn. 1, 349-369.
66. Spiegler, B.J., and Mishkin, M. (1981). Evidence for the sequential participation of inferior temporal cortex and amygdala in the acquisition of stimulus-reward associations. Behav. Brain Res. 3, 303-317.
67. Talairach, J., and Tournoux, P. (1988). Co-planar Stereotaxic Atlas of the Human Brain (New York: Thieme Medical Publishers).
68. Tomkins, S.S. (1962). Affect Imagery Consciousness, Volume 1: The Positive Affects (New York: Springer Publishing).
69. Tomkins, S.S. (1963). Affect Imagery Consciousness, Volume 2: The Negative Affects (New York: Springer Publishing).
70. Tootell, R.B.H., Reppas, J.B., Kwong, K.K., Malach, R., Born, R.T., Brady, T.J., Rosen, B.R., and Belliveau, J.W. (1995). Functional analysis of human MT and related visual cortical areas using magnetic resonance imaging. J. Neurosci. 15, 3215-3230.
71. Woods, R.P., Cherry, S.R., and Mazziotta, J.C. (1992). Rapid automated algorithm for aligning and reslicing PET images. J. Comp. Assist. Tomogr. 16, 620-633.