Effects of aspiration versus neurotoxic lesions of the amygdala on emotional responses in monkeys

European Journal of Neuroscience

Volumn 11, Issue 12, 1999, Pages 4403-4418

  Meunier, Martine ^b   Bachevalier, Jocelyne ^c   Murray, Elisabeth A ^a   Málková, Ludiše ^d   Mishkin, Mortimer ^a  

^a NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^b CNRS   (France)

^c UNIVERSITY OF TEXAS   (United States)

^d GEORGETOWN UNIVERSITY   (United States)

Author keywords

Emotions; Ibotenic acid lesions; Medial temporal cortex; Rhesus macaques; Rhinal cortex

Indexed keywords

AGGRESSION; AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASPIRATION; CONTROLLED STUDY; EMOTION; FEAR; MALE; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; RHESUS MONKEY; TEMPORAL CORTEX;

AFFECTIVE SYMPTOMS; AGGRESSION; AMYGDALA; ANIMALS; BEHAVIOR, ANIMAL; DOMINANCE-SUBORDINATION; FEAR; IBOTENIC ACID; MACACA MULATTA; MAGNETIC RESONANCE IMAGING; MALE; PHOTIC STIMULATION; PHYSICAL STIMULATION;

EID: 0033404851     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.1999.00854.x     Document Type: Article

References (71)

1. Akert, K., Gruesen, R.A., Woolsey, C.N. & Meyer, D.R. (1961) Klüver-Bucy syndrome in monkeys with neocortical ablations of temporal lobe. Brain, 84, 480-498.
2. Adolphs, R., Tranel, D., Damasio, H. & Damasio, A.R. (1994) Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala. Nature, 372, 669-672.
3. Aggleton, J.P. (1992) The functional effects of amygdala lesions in humans, a comparison with findings from monkeys. In Aggleton, J.P. (ed.), The Amygdala. Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction. Wiley-Liss, New York, pp. 485-504.
4. Aggleton, J.P. & Passingham, R.E. (1981) Syndrome produced by lesions of the amygdala in monkeys (Macaca mulatta). J. Comp. Physiol. Psychol., 95, 961-977.
5. Aggleton, J.P. & Passingham, R.E. (1982) An assessment of the reinforcing properties of foods after amygdaloid lesions in rhesus monkeys. J. Comp Physiol. Psychol., 95, 961-977.
6. Baxter, M.G., Saunders, R.C. & Murray, E.A. (1998) Aspiration lesions of the amygdala interrupt connections between prefrontal cortex and temporal cortex in rhesus monkeys. Soc. Neurosci. Abstr., 24, 1905.
7. Breiter, H.C., Etcoff, N.L., Whalen, P.J., Kennedy, W.A., Rauch, S.L., Buckner, R.L., Strauss, M.M., Hyman, S.E. & Rosen, B.R. (1996) Response and habituation of the human amygdala during visual processing of facial expression. Neuron, 17, 875-887.
8. Broks, P., Young, A.W., Maratos, E.J., Coffey, P.J., Calder, A.J., Isaac, C.L., Mayes, A.R., Hodges, J.R., Montaldi, D., Cezayirli, E., Roberts, N. & Hadley, D. (1998) Face processing impairments after encephalitis: amygdala damage and recognition of fear. Neuropsychologia, 36, 59-70.
9. Butter, C.M., Mishkin, M. & Mirsky, A.F. (1967) Emotional responses toward humans in monkeys with selective frontal lesions. Physiol. Behav., 3, 213-215.
10. Cahill, L., Babinsky, R., Markowitsch, H.J. & McGaugh, J.L. (1995) The amygdala and emotional memory. Nature, 377, 295-296.
11. Capitano, J.P. (1986) Behavioral pathology. In Mitchell, G. & Erwin, J. (eds) Comparative Primate Biology Vol. 2A, Behavior, Conservation, and Ecology. Allan R. Liss, New York, pp. 411-454.
12. Chevalier-Skolnikoff, S. (1973) Facial expression of emotion in primates. In Ekman, P. (ed.) Darwin and Facial Expression: A Century of Research in Review. Academic Press, New York, pp. 11-89.
13. Corwin, J.V., Vicedomini, J.P., Nonneman, A.J. & Valentino, L. (1982) Serial lesion effect in rat medial frontal cortex as a function of age. Neurobiol. Aging, 3, 69-76.
14. Davis, M. (1992) The role of the amygdala in conditioned fear. In Aggleton, J.P. (ed.), The Amygdala. Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction. Wiley-Liss, New York, pp. 255-305.
15. De Waal, F. (1989) Peacemaking Among Primates. Harvard University Press, Cambridge, MA, USA.
16. Dunn, L.T. & Everitt, B.J. (1988) Double dissociations of the effects of amygdala and insular cortex lesions on conditioned taste aversion, passive avoidance, and neophobia in the rat using the excitotoxin ibotenic acid. Behav. Neurosci., 102, 3-23.
17. Franzen, E.A. & Myers, R.E. (1973) Neural control of social behavior: prefrontal and anterior temporal cortex. Neuropsychologia, 11, 141-157.
18. Fried, I., MacDonald, K.A. & Wilson, C.L. (1997) Single neuron activity in human hippocampus and amygdala during recognition of faces and objects. Neuron, 18, 753-765.
19. Gaffan, E.A., Gaffan, D. & Harrison, S. (1988) Disconnection of the amygdala from visual association cortex impairs visual reward-association learning in monkeys. J. Neurosci., 8, 3144-3150.
20. Gallagher, M. & Chiba, A.A. (1996) The amygdala and emotion. Curr. Opin. Neurobiol., 6, 221-227.
21. Gallagher, M. & Holland, P.C. (1994) The amygdala complex: multiple roles in associative learning and attention. Proc. Natl Acad. Sci., USA, 91, 11771-11776.
22. Goosen, C. (1981) Abnormal behavior patterns in rhesus monkeys: symptoms of mental disease? Biol. Psychiatry, 16, 697-716.
23. Goulet, S., Doré, F.Y. & Murray, E.A. (1998) Aspiration lesions of the amygdala disrupt the rhinal corticothalamic projection system in rhesus monkeys. Exp. Brain Res., 119, 131-140.
24. Hinde, R.A. & Rowell, T.E. (1962) Communication by postures and facial expressions in the rhesus monkey (Macaca mulatta). Proc. Zool. Soc. Lond., 138, 1-21.
25. Hodos, W. & Bobko, P. (1984) A weighed index of bilateral brain lesions. J. Neurosci. Meth, 12, 43-47.
26. Horel, J.A., Keating, E.G. & Misantone, L.J. (1975) Partial Klüver-Bucy syndrome produced by destroying temporal neocortex or amygdala. Brain Res., 94, 347-359.
27. Horel, J.A. & Misantone, L.J. (1974) The Klüver-Bucy syndrome produced by partial isolation of the temporal lobe. Exp. Neurol., 42, 101-112.
28. Iwai, E., Nishio, T. & Yamaguchi, K. (1986) Neuropsychological basis of a K-B sign in Klüver-Bucy syndrome produced following total removal of inferotemporal cortex of macaque monkeys. In Oomura, Y. (ed.). Emotion: Neural and Chemical Control. Japan Scientific Society Press, Tokyo, pp. 299-311.
29. Jones, B. & Mishkin, M. (1972) Limbic lesions and the problem of stimulus-reinforcement associations. Exp. Neurol., 36, 362-377.
30. Kalin, N.D., Shelton, S.E. & Takahashi, L.K. (1991) Defensive behaviors in infant rhesus monkeys: their ontogeny and context-dependent selective expression. Child Dev., 62, 1175-1183.
31. Kaufman, C. & Rosenblum, L.A. (1966) A behavioral taxonomy for Macaca Nemestrina and Macaca Radiata based on longitudinal observation of family groups in the laboratory. Primates, 7, 205-254.
32. Kenney, M.D., Mason, W.A. & Hill, S.D. (1979) Effects of age, objects, and visual experience on affective responses of rhesus monkeys to strangers. Develop. Psychol., 15, 176-184.
33. Killcross, S., Robbins, T.W. & Everitt, B.J. (1997) Different types of fear-conditioned behavior mediated by separate nuclei within the amygdala. Nature, 388, 377-380.
34. Kling, A.S. & Brothers, L.A. (1992) The amygdala and social behavior. In Aggleton, J.P. (ed.), The Amygdala. Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction. Wiley-Liss, New York, pp. 353-378.
35. Kling, A.S., Tachiki, K. & Loyd, R. (1993) Neurochemical correlates of the Klüver-Bucy syndrome by in vivo microdialysis in monkey. Behav. Brain Res., 56, 161-170.
36. Klüver, H. & Bucy, P.C. (1938) An analysis of certain effects of bilateral temporal lobectomy in the rhesus monkey, with special reference to 'psychic blindness'. J. Psychol., 5, 33-54.
37. Klüver, H. & Bucy, P.C. (1939) Preliminary analysis of functions of the temporal lobes in monkeys. Arch. Neurol. Psychiat., 42, 979-1000.
38. LeDoux, J.E. (1992) Emotion and the amygdala. In Aggleton, J.P. (ed.), The Amygdala. Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction. Wiley-Liss, New York, pp. 339-351.
39. Maestripieri, D. & Wallen, K. (1997) Affiliative and submissive communication in rhesus macaques. Primates, 38, 127-138.
40. Málková, L., Gaffan, D. & Murray, E.A. (1997) Excitotoxic lesions of the amygdala fail to produce impairment in visual learning for auditory secondary reinforcement but interfere with reinforcer devaluation effects in rhesus monkeys. J. Neurosci., 17, 6011-6020.
41. McGaugh, J.L., Entroini-Collison, I.B., Cahill, L., Kim, M. & Liang, K.C. (1992) Involvement of the amygdala in neuromodulatory influences on memory storage. In Aggleton, J.P. (ed.) The Amygdala. Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction. Wiley-Liss, New York, pp. 431-452.
42. McIntyre, M. & Stein, D.G. (1973) Differential effect of one-stage vs two-stage amygdaloid lesions on activity, exploratory, and avoidance behavior in the albino rat. Exp. Neurol., 40, 263-277.
43. Meunier, M., Bachevalier, J., Mishkin, M. & Murray, E.A. (1993) Effects on visual recognition of combined and separate ablations of the entorhinal and perirhinal cortex in rhesus monkeys. J. Neurosci., 13, 5418-5432.
44. Meunier, M., Bachevalier, J., Murray, E.A., Málková, L. & Mishkin, M. (1996) Effects of aspiration vs neurotoxic lesions of the amygdala on emotional reactivity in rhesus monkeys. Soc. Neurosci. Abstr., 22, 1867.
45. Meunier, M., Bachevalier, J., Murray, E.A., Merjanian, P.M. & Richardson, R. (1991) Effects of rhinal cortical or limbic lesions on fear reactions in rhesus monkeys. Soc. Neurosci. Abstr., 17, 337.
46. Meyer, D.R. (1972) Some features of the dorsolateral frontal and inferotemporal syndromes in monkeys. Acta Neurobiol. Exp. (Warszawa), 32, 235-260.
47. Mineka, S. & Cook, M. (1988) Social learning and the acquisition of snake fear in monkeys. In Zentall, T. & Galef, B. (eds), Social Learning: Psychological and Biological Perspectives. Erlbaum, Hillsdale, NJ, pp. 51-73.
48. Mineka, S., Keir, R. & Price, V. (1980) Fear of snakes in wild- and lab-reared rhesus monkeys. Anim. Learn. Behav., 8, 653-663.
49. Morris, J.S., Ohman, A. & Dolan, R.J. (1998) Conscious and unconscious emotional learning in the human amygdala. Nature, 393, 467-470.
50. Murray, E.A. (1987) Normal learning set formation in monkeys with combined ablation of the amygdaloid complex and hippocampal formation. Soc. Neurosci. Abstr., 13, 206.
51. Murray, E.A. (1996) What have ablation studies told us about the neural substrates of stimulus memory. Sem. Neurosci., 8, 13-22.
52. Murray, E.A. & Gaffan, D. (1994) Removal of the amygdala plus subjacent cortex disrupts the retention of both intramodal and crossmodal associative memories in monkeys. Behav. Neurosci., 108, 494-500.
53. Murray, E.A., Gaffan, E.A. & Flint, R.W. Jr (1996) Anterior rhinal cortex and amygdala: dissociation of their contributions to memory and food preference in rhesus monkeys. Behav. Neurosci., 110, 30-42.
54. Murray, E.A., Gaffan, D. & Mishkin, M. (1993) Neural substrates of visual stimulus-stimulus association in rhesus monkeys. J. Neurosci., 13, 4549-4561.
55. Myers, R.E. & Swett, C. (1970) Social behavior deficits of free-ranging monkeys after anterior temporal cortex removal: a preliminary report. Brain Res., 18, 551-556.
56. Phelps, E.A., LaBar, K.S. & Spencer, D.D. (1997) Memory for emotional words following unilateral temporal lobectomy. Brain Cogn., 35, 85-109.
57. Potegal, M., Ferris, C.F., Hebert, M., Meyerhoff, J. & Skaredoff, L. (1996) Attack priming in female Syrian golden hamsters is associated with a c-fos-coupled process within the corticomedial amygdala. Neuroscience, 75, 869-880.
58. Raleigh, M.J. & Steklis, H.D. (1981) Effects of orbitofrontal and temporal neocortical lesions on the affiliative behavior of Vervet monkeys (Cercopithecus aethiops sabaeus). Exp. Neurol., 73, 378-389.
59. Rosvold, H.E., Mirsky, A.F. & Pribram, K. (1954) Influence of amygdalectomy on social behavior in monkeys. J. Comp. Physiol. Psychol., 47, 173-178.
60. Sade, D.S. (1973) An ethogram for rhesus monkeys. I. Antithetical contrasts in posture and movement. Am. J. Phys. Anthrop., 38, 537-542.
61. Salinas, J.A., Parent, M.B. & McGaugh, J.L. (1996) Ibotenic acid lesions of the amygdala basolateral complex and central nucleus differentially effect the response to reductions in reward. Brain Res., 742, 283-293.
62. Scott, S.K., Young, A.W., Calder, A.J., Hellawell, D.J., Aggleton, J.P. & Johnson, M. (1997) Impaired auditory recognition of fear and anger following bilateral amygdala lesions. Nature, 385, 254-257.
63. Spiegler, B.J. & 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.
64. Stark, C.P., Alpern, H.P., Fuhrer, J., Trowbridge, M.G., Wimbish, H. & Smock, T. (1998) The medial amygdaloid nucleus modifies social behavior in male rats. Physiol. Behav., 63, 253-259.
65. Suomi, S.J. (1982) Abnormal behavior and primate models of psychopathology. In Fobes, J.L. & Kling, J.E. (eds) Primate Behavior. Academic Press, New York, pp. 171-215.
66. von Bonin, G. & Bailey, P. (1947) The Neocortex of Macaca Mulatta. University of Illinois, Urbana, IL, USA.
67. Walker, A.E., Thomson, A.F. & McQueen, J.D. (1953) Behavior and the temporal rhinencephalon in the monkeys. Johns Hopkins Hosp. Bull., 49, 381-391.
68. Weiskrantz, L. (1956) Behavioral changes associated with ablation of the amygdaloid complex in monkeys. J. Comp. Physiol. Psychol., 49, 381-391.
69. Whalen, P.J., Rauch, S.L., Etcoff, N.L., McInerney, S.C., Lee, M.B. & Jenike, M.A. (1998) Masked presentations of emotional facial expressions modulate amygdala activity without explicit knowledge. J. Neurosci., 18, 411-418.
70. Zald, D.H. & Pardo, J.V. (1997) Emotion, olfaction, and the human amygdala, amygdala activation during aversive olfactory stimulation. Proc. Natl Acad. Sci. USA, 94, 119-124.
71. Zola-Morgan, S., Squire, L.R., Alvarez-Royo, P. & Clower, R.P. (1991) Independence of memory functions and emotional behavior: separate contributions of the hippocampal formation and the amygdala. Hippocampus, 1, 207-220.