Effects of orbital frontal and anterior cingulate lesions on object and spatial memory in rhesus monkeys

Neuropsychologia

Volumn 35, Issue 7, 1997, Pages 999-1015

  Meunier, Martine ^a,b   Bachevalier, Jocelyne ^a,c   Mishkin, Mortimer ^a,d  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b UNIVERSITÉ DE BORDEAUX   (France)

^c UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^d NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

Author keywords

Delayed nonmatching to sample; Discrimination reversal learning; Memory; Nonhuman primates; Prefrontal cortex; Spatial delayed response

Indexed keywords

AMNESIA; ANIMAL EXPERIMENT; ARTICLE; ASSOCIATION; BRAIN INJURY; CINGULATE GYRUS; CONTROLLED STUDY; FEMALE; FRONTAL CORTEX; LEARNING; MALE; NONHUMAN; RECOGNITION; RHESUS MONKEY; SPATIAL MEMORY;

ANIMALS; BRAIN MAPPING; DISCRIMINATION LEARNING; FEMALE; GYRUS CINGULI; LIMBIC SYSTEM; MACACA MULATTA; MALE; MENTAL RECALL; NERVE NET; NEURAL PATHWAYS; ORIENTATION; PATTERN RECOGNITION, VISUAL; PREFRONTAL CORTEX;

EID: 0030844802     PISSN: 00283932     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0028-3932(97)00027-4     Document Type: Article

References (80)

1. Aggleton, J. P., Desimone, R. and Mishkin, M. The origin, course, and termination of the hippocampothalamic projections in the macaque. Journal of Comparative Neurology 243, 409-421, 1986.
2. Aggleton, J. P., Hunt, P. R. and Rawlins, J. N. P. The effects of hippocampal lesions upon spatial and non-spatial tests of working memory. Behavioral Brain Research 19, 133-146, 1986.
3. Aggleton, J. P. and Mishkin, M. Visual recognition impairment following medial thalamic lesions in monkeys. Neuropsychologia 21, 189-197, 1983.
4. Aggleton, J. P. and Mishkin, M. Memory impairments following restricted medial thalamic lesions in monkeys. Experimental Brain Research 52, 199-209, 1983.
5. Aggleton, J. P. and Mishkin, M. Projections of the amygdala to the thalamus in the cynomolgus monkey. Journal of Comparative Neurology 222, 56-68, 1984.
6. Aggleton, J. P., Neave, N., Nagle, S. and Sahgal, A. A comparison of the effects of medial prefrontal, cingulate cortex, and cingulum bundle lesions on tests of spatial memory: Evidence of a double-dissociation between frontal and cingulum bundle contributions. Journal of Neuroscience 15, 7270-7281, 1995.
7. Alvarez, P., Zola-Morgan, S. and Squire, L. R. Damage limited to the hippocampal region produces longlasting memory impairment in monkeys. Journal of Neuroscience 15, 3796-3807, 1995.
8. Arikuni, T., Sako, H. and Murata, A. Ipsilateral connections of the anterior cingulate cortex with the frontal and medial temporal cortices in the macaque monkey. Neuroscience Research 21, 19-39, 1994.
9. Bachevalier, J., tandis, L. S., Walker, L. C, Brick-son, M.. Mishkin, M., Price, D. L. and Cork, L. C. Aged monkeys exhibit behavioral deficits indicative of widespread cerebral dysfunction. Neurobiologv of Aging 12, 99-111, 1991.
10. Bachevalier, J. and Mishkin, M. Visual recognition impairment follows ventromedial but not dorsolateral prefrontal lesions in monkeys. Behavioral Brain Research 20, 249-261, 1986.
11. Bachevalier, J., Parkinson, J. K. and Mishkin, M. Visual recognition in monkeys: Effects of separate versus combined transection of fornix and amygdalofugal pathways. Experimental Brain Research 57,554-561, 1985.
12. Baleydier. C. and Mauguiere, F. The duality of the cingulate gyrus in monkey: Neuroanatomical study and functional hypothesis. Brain 103, 525-554, 1980.
13. Barbas. H., Haswell, T. H. and Dermon, C. R. Diverse thalamic projections to the prefrontal cortex in the rhesus monkey. Journal of Comparative Neurology 313,65-94, 1991.
14. Barbas, H. and Pandya, D. N. Architecture and intrinsic connections of the prefrontal cortex in the rhesus monkey. Journal of Comparative Neurology 286,353-375,1989.
15. Battig, K., Rosvold, H. E. and Mishkin, M. Comparison of the effects of frontal and caudate lesions on delayed response and alternation in monkeys. Journal of Comparative Physiology and Psychology 53,400-404,1960.
16. Baylis, L. L., Rolls, E. T. and Baylis, G. C. Afferent connections of the caudolateral orbitofrontal cortex taste area of the primate. Neuroscience 64, 801-812, 1995.
17. Cirillo. R. A., Horel, J. A. and George, P. J. Lesions of the anterior temporal stem and performance of delayed match-to-sample and visual discrimination in monkeys. Behavioral Brain Research 34, 55-69, 1989.
18. Deuel, R. K. and Mishkin, M. Limbic and prefrontal contributions to somesthesic learning in monkeys. Brain Research 132, 521-536, 1977.
19. Eacott. M. J., Gaffan, D. and Murray, E. A. Preserved recognition memory for small sets, and impaired stimulus identification for large sets, following rhinal cortex ablations in monkeys. European Journal of Neuroscience 6, 1466-1478, 1994.
20. Gaffan, D. Recognition impaired and association intact in the memory of monkeys with transection of the fornix. Journal of Comparative Physiology and Psychology 86, 1100-1109, 1974.
21. Gaffan, D. and Eacott, M. J. Uncinate fascicle section leaves delayed matching-to-sample intact, with both large and small stimulus set. Experimental Brain Research 105, 175-180, 1995.
22. Gaffan, D., Murray, E. A. and Fabre-Thorpe, M. Interaction of the amygdala with the frontal lobe in reward memory. European Journal of Neuroscience 5, 968-975, 1993.
23. George, P. J., Horel, J. A. and Cirillo, R. A. Reversible cold lesions of the parahippocampal gyrus in monkeys results in deficits on the delayed matchto-sample and other visual tasks. Behavioral Brain Research 34, 163-178, 1989.
24. Goldman-Rakic, P. S. and Porrino, L. J. The primate mediodorsal nucleus and its projection to the frontal lobe. Journal of Comparative Neurologv 242, 535-560, 1985.
25. Horel, J. A., Pytko-Joiner, D. E., Voytko, M. L. and Salsbury, K. The performance of visual tasks while segments of the inferotemporal cortex are suppressed by cold. Behavioral Brain Research 23, 29-42, 1987.
26. Iversen, S. D. and Mishkin, M. Perseverative interference in monkeys following selective lesions of the inferior prefrontal convexity. Experimental Brain Research 11, 376-386, 1970.
27. Jones, B. and Mishkin, M. Limbic lesions and the problem of stimulus-reinforcement associations. Experimental Neurology 36, 362-377, 1972.
28. Jones-Gotman, M. and Zatorre. R. J. Odor recognition memory in humans: Role of right temporal and orbitofrontal regions. Brain and Cognition 22, 182-198, 1993.
29. Kievit. J. and Kuypers. H. G. J. Organization of the thalamocortical connections to the frontal lobe in rhesus monkey. Experimental Brain Research 29, 299-322, 1977.
30. Kowalska, D. M., Bachevalier, J. and Mishkin, M. The role of the inferior prefrontal convexity in performance of delayed nonmatching-to-sample. Neuropsychologia 29, 583-600, 1991.
31. Markowska. A. L., Olton, D. S., Murray. E. A. and Gaffan, D. A comparative analysis of the role of fornix and cingulate cortex in memory: Rats. Experimental Brain Research 74, 187 201, 1989.
32. Martin-Helkins, C. L. and Horel, J. A. Cortical afferents to behaviorally denned regions of the inferior temporal and parahippocampal gyri as demonstrated by WGA-HRP. Journal of Comparative Neurology 321, 177-192, 1992.
33. Matelli, M., Luppino. G. and Rizzolatti, G. Architecture of superior and mesial area 6 and the adjacent cingulate cortex in the macaque monkey. Journal of Comparative Neurology 311, 445-462, 1991.
34. Meunier, M., Bachevalier, B.. Mishkin, M. and Murray, E. A. Effects on visual recognition of combined and separate ablations of the entorhinal and perirhinal cortex in rhesus monkeys. Journal of 'Ne uroscience 13, 5418-5432. 1993.
35. Meunier. M. and Destrade, C. Electrolytic but not ibotenic acid lesions of the posterior cingulate cortex produce transitory facilitation of learning in mice. Behavioral Brain Research 27, 161-172. 1988.
36. Meunier. M.. Jaffard, R. and Destrade, C. Differential involvement of anterior and posterior cingulate cortices in spatial discriminative learning in a Tmaze in mice. Behavioral Brain Research 44, 133-143, 1991.
37. Mishkin. M. Memory in monkeys severely impaired by combined but not by separate removal of the amygdala and hippocampus. Nature 273, 297-298, 1978.
38. Mishkin. M. and Delacour, J. An analysis of shortterm visual memory in the monkey. Journal of Experimental Psychology 1, 326-333. 1975.
39. Morecraft. R. J.. Geula. C. and Mesulam, M. M. Cytoarchitecture and neural afferents of orbito-frontal cortex in the brain of the monkey. Journal of Comparative Neurology 323, 341-358, 1992.
40. Mumby, D. G. and Pinel, J. P. J. Rhinal cortex lesions and object recognition in rats. Behavioral Neuroscience 108, 1-8, 1994.
41. Mumby, D. G., Wood, E. R. and Pinel, J. P. J. Object-recognition memory is only mildly impaired in rats with lesions of the hippocampus and amygdala. Psychobiology 20, 18-27, 1992.
42. Murray, E. A., Medial temporal lobe structures contributing to recognition memory: The amygdaloid complex versus the rhinal cortex. In The Amygdala: Neurobiological Aspects of Emotion, Memory and Mental Dysfunction, ed. J. P. Aggleton. Wiley-Liss, New York, 1992, pp. 453-470.
43. Murray, E. A., Davidson, M., Gaffan, D., Olton, D. S. and Suomi, S. Effects of fornix transection and cingulate cortical ablation on spatial memory in rhesus monkeys. Experimental Brain Research 74, 173-186, 1989.
44. Murray, E. A. and Mishkin, M. Severe tactual as well as visual memory deficits follow combined removal of the amygdala and hippocampus in monk-eys. Journal of Neuroscience 4, 2565-2580, 1984.
45. Murray, E. A. and Mishkin, M. Visual recognition in monkeys following rhinal cortical ablations combined with either amygdalectomy or hippo-campectomy. Journal of Neuroscience 6, 1991-2003, 1986.
46. Neave, S., Lloyd, S., Sahgal, A. and Aggleton, J. P. Lack of effect of lesions in the anterior cingulate cortex and retrosplenial cortex on certain tests of spatial memory in the rat. Behavioral Brain Research 65,89-101, 1994.
47. Niki, H. and Watanabe, M. Cingulate unit activity and delayed response. Brain Research 110, 381-386, 1976.
48. O'Boyle, V. J.Jr., Murray, E. A. and Mishkin, M. Effects of excitotoxic amygdalohippocampal lesions on visual recognition in rhesus monkeys. Soc. Neuroscience Abstracts 19, 438, 1993.
49. Otto, T. and Eichenbaum, H. Complementary roles of the orbital prefrontal cortex and the perirhinalentorhinal cortices in an odor-guided delayed-nonmatching-to-sample. Behavioral Neuroscience 106, 762-775, 1992.
50. Porrino, L. P., Crane, A. M. and Goldman-Rakic, P. S. Direct and indirect pathways from the amygdala to the frontal lobe in rhesus monkeys. Journal of Comparative Neurology 198, 121-136, 1981.
51. Pribram, K. H., Wilson, W. A. and Connors, J. Effects of lesions of the medial forebrain on alternation behavior of rhesus monkeys. Experimental Neurology 6, 36-47, 1962.
52. Ray, J. P. and Price, J. L. The organization of projections from the mediodorsal nucleus of the thalamus to orbital and medial prefrontal cortex in macaque monkeys. Journal of Comparative Neurology 337, 1-31, 1993.
53. Rolls, E. T. and Baylis, L. L. Gustatory, olfactory, and visual convergence within the primate orbitofrontal cortex. Journal of Neuroscience 14, 5437-5452, 1994.
54. Rolls, E. T., Critchley, H. D., Mason, R. and Wakeman, E. A., Orbitofrontal cortex neurons: Role in olfactory and visual association learning. Journal of Neurophvsiology 75, 1982-1986, 1996.
55. Rolls, E. T., Hornak, J., Wade, D. and McGrath, J. Emotion-related learning in patients with social and emotional changes associated with frontal lobe damage. Journal of Neurology, Neurosurgery and Psychiatry 57, 1518-1524, 1994.
56. Rolls, E. T., Yaxley, S. and Sienkiewicz, Z. J. Gustatory responses of single neurons in the orbitofrontal cortex of the macaque monkey. Journal of Neurophysiology 64, 1055-1066, 1990.
57. Rosenkilde, C. E., Bauer, R. H. and Fuster, J. M. Single cell activity in ventral prefrontal cortex of behaving monkeys. Brain Research 209, 375-394, 1981.
58. Rothblat, L. A. and Kromer, F. K. Object recognition memory in the rat: The role of the hippocampus. Behavioral Brain Research 42, 25-32, 1991.
59. Russchen, F. T., Amaral, D. G. and Price, J. L. The afferent input to the magnocellular division of the mediodorsal thalamic nucleus in the monkey Macaca fascicularis. Journal of Comparative Neurology 256, 175-210, 1987.
60. Saunders, R. C., Murray, E. A. and Mishkin, M. Further evidence that amygdala and hippocampus contribute equally to recognition memory. Neuropsychologia 22, 785-796, 1984.
61. Schoenbaum, G. and Eichenbaum, H. Information coding in the rodent prefrontal cortex: I. Single neuron activity in orbitofrontal cortex compared with that in pyriform cortex. Journal of Neurophysiologv 74,733-750,1995.
62. Schoenbaum, G. and Eichenbaum, H. Information coding in the rodent prefrontal cortex: II. Ensemble activity in orbitofrontal cortex. Journal of Neurophysiologv 74, 751-762, 1995.
63. Sutherland, R. J., Whishaw, I. Q. and Kolb, B. Contributions of cingulate cortex to two forms of spatial learning and memory. Journal of Neuroscience 8, 1863-1872, 1988.
64. Suzuki, W. A. and Amaral, D. G. Perirhinal and parahippocampal cortices of the macaque monkey: Cortical afferents. Journal of Comparative Neurologv 350,497-533,1994.
65. Suzuki, W. A., Zola-Morgan, S., Squire, L. R. and Amaral, D. G., Lesions of the perirhinal and parahippocampal cortices in the monkey produce long lasting memory impairments in the visual and tactual modalities. Journal of Neuroscience 13, 2430-2451, 1993.
66. Takagi, S. F. The olfactory nervous system of the Old World monkey. Jpn. Journal of Physiology 34, 561-573, 1984.
67. Takagi, S. F. Studies on the olfactory nervous system of the Old World monkey. Progress in Neurobiology 27, 195-250, 1986.
68. Tanabe, T., lino, M. and Takagi, S. F. Discrimination of odors in olfactory bulb, pyriform amygdaloid areas, and orbitofrontal cortex of the monkey. Journal of Neurophysiology 38, 1284-1296, 1975.
69. Tanabe, T., Yarita, H., lino, M., Ooshima, Y. and Takagi, S. F. An olfactory projection area in orbitofrontal cortex of the monkey. Journal of Neurophvsiologv 38, 1269-1283, 1975.
70. Thorpe. S.J., Rolls, E. T. and Maddison, S. The orbitofrontal cortex: Neuronal activity in the behaving monkey. Experimental Brain Research 49, 93-115. 1983.
71. Ungerleider, L. G., Gaffan. D. and Pelak, V. S. Projections from inferior temporal cortex to prefrontal cortex via the uncinate fascicle in rhesus monkeys. Experimental Brain Research 76, 473-484, 1989.
72. Van Hoesen, G. W., Pandya, D. N. and Butters, N. Some connections of the entorhinal (area 28) and perirhinal (area 35) cortices of the rhesus monkey: II. Frontal lobe afferents. Brain Research 95, 25-38. 1975.
73. Vogt, B. A.. Pandya, D. N. and Rosene, D. L. Cingulate cortex of the rhesus monkey: I. Cytoarchitecture and thalamic afferents. Journal of Comparative Neurology 262,256-270, 1987.
74. Voytko. M. L. Cooling orbital frontal cortex disrupts matching-to-sample and visual discrimination learning in monkeys. Phvsiologv and Psychologv 13, 219229. 1985.
75. Webster, ML J., Bachevalier, J. and Ungerleider, L. G. Connections of inferior temporal areas TEO and TE with parietal and frontal cortex in macaque monkeys. Cerebral Cortex 5, 470-483, 1994.
76. Yarita, H., lino, M., Tanabe. T., Kogure. S. and Takagi. S. F. A transthalamic olfactory pathway to orbitofrontal cortex in the monkey. Journal of Neurophysiology 43, 69-85, 1980.
77. Zola-Morgan, S. and Squire, L. R. Amnesia in monkeys following lesions of the mediodorsal nucleus of the thalamus. Ann. Neurology 17, 558-564, 1985.
78. Zola-Morgan. S., Squire, L. R. and Amaral, D. G. Lesions of the amygdala that spare the adjacent cortical regions do not impair memory or exacerbate the impairment following lesions of the hippocampal formation. Journal of Neuroscience 9, 1922-1936, 1989.
79. Zola-Morgan, S., Squire, L. R.. Amaral, D. G. and Suzuki, W. A. Lesions of the perirhinal and parahippocampal cortex that spare the amygdala and hippocampal formation produce severe memory impairment. Journal of Neuroscience 9, 4355- 4370. 1989.
80. Zola-Morgan, S., Squire, L. R.. Glower, R. P. and Rempel, N. L. Damage to the perirhinal cortex exacerbates memory impairment following lesions of the hippocampal formation. Journal of Neuroscience 13,251-265,1993.