Lesions of the perirhinal and parahippocampal cortices in the monkey produce long-lasting memory impairment in the visual and tactual modalities

Compared to normal animals, monkeys with bilateral lesions of the perirhinal and parahippocampal cortices (PRPH lesion) were impaired on both a visual and a tactual version of the delayed nonmatching to sample task. In addition, the memory deficit was long-lasting, as indicated by the finding of a significant deficit when the visual version of the delayed nonmatching to sample task was readministered approximately 2 years after surgery. Animals with PRPH lesions performed normally on discrimination tasks in the visual and tactual modalities. Multimodal and long-lasting memory impairments are defining characteristics of human medial temporal lobe amnesia. Accordingly, these results demonstrate important parallels between the memory deficit associated with PRPH lesions and human medial temporal lobe amnesia. These data, taken together with previous findings, suggest that the perirhinal and parahippocampal cortices play an important role in memory function and that these cortical areas are critical components of the medial temporal lobe memory system.

[1]  D. Amaral,et al.  The entorhinal cortex of the monkey: II. Cortical afferents , 1987, The Journal of comparative neurology.

[2]  Louis W. Gellermann Chance Orders of Alternating Stimuli in Visual Discrimination Experiments , 1933 .

[3]  M. Mishkin,et al.  Severe tactual as well as visual memory deficits follow combined removal of the amygdala and hippocampus in monkeys , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  Leslie G. Ungerleider,et al.  Connections of inferior temporal areas TE and TEO with medial temporal- lobe structures in infant and adult monkeys , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[5]  B. Milner,et al.  Further analysis of the hippocampal amnesic syndrome: 14-year follow-up study of H.M.☆ , 1968 .

[6]  J. Maunsell,et al.  Two‐dimensional maps of the cerebral cortex , 1980, The Journal of comparative neurology.

[7]  W. Scoville,et al.  LOSS OF RECENT MEMORY AFTER BILATERAL HIPPOCAMPAL LESIONS , 1957, Journal of neurology, neurosurgery, and psychiatry.

[8]  G. J. Romanes,et al.  The Neocortex of Macaca mulatta , 1948 .

[9]  H Eichenbaum,et al.  Further studies of hippocampal representation during odor discrimination learning. , 1989, Behavioral neuroscience.

[10]  L. Squire,et al.  Human amnesia and animal models of amnesia: performance of amnesic patients on tests designed for the monkey. , 1988, Behavioral neuroscience.

[11]  Y. Miyashita,et al.  Neuronal correlate of pictorial short-term memory in the primate temporal cortexYasushi Miyashita , 1988, Nature.

[12]  L. Squire,et al.  Preserved learning in monkeys with medial temporal lesions: sparing of motor and cognitive skills , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  L. Squire,et al.  Lesions of the amygdala that spare adjacent cortical regions do not impair memory or exacerbate the impairment following lesions of the hippocampal formation , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  D. Amaral,et al.  Lesions of perirhinal and parahippocampal cortex that spare the amygdala and hippocampal formation produce severe memory impairment , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  H. Eichenbaum,et al.  Complementary roles of the orbital prefrontal cortex and the perirhinal-entorhinal cortices in an odor-guided delayed-nonmatching-to-sample task , 1992 .

[16]  M. Mesulam,et al.  Insula of the old world monkey. III: Efferent cortical output and comments on function , 1982, The Journal of comparative neurology.

[17]  G A Press,et al.  Magnetic resonance imaging of the hippocampal formation and mammillary nuclei distinguish medial temporal lobe and diencephalic amnesia , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[18]  H. Eichenbaum,et al.  Hippocampal representation in place learning , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  L. Squire,et al.  Human amnesia and the medial temporal region: enduring memory impairment following a bilateral lesion limited to field CA1 of the hippocampus , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  M. Mishkin,et al.  Visual recognition impairment following medial thalamic lesions in monkeys , 1983, Neuropsychologia.

[21]  B. Milner,et al.  Disorders of learning and memory after temporal lobe lesions in man. , 1972, Clinical neurosurgery.

[22]  M. Victor,et al.  Amnesia due to Lesions Confined to the Hippocampus: A Clinical-Pathologic Study , 1990, Journal of Cognitive Neuroscience.

[23]  L. Squire,et al.  Memory impairment in monkeys following lesions limited to the hippocampus. , 1986, Behavioral neuroscience.

[24]  L. Squire,et al.  Enduring memory impairment in monkeys after ischemic damage to the hippocampus , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  D. Pandya,et al.  Some cortical projections to the parahippocampal area in the rhesus monkey , 1976, Experimental Neurology.

[26]  D. Amaral,et al.  Entorhinal cortex of the monkey: V. Projections to the dentate gyrus, hippocampus, and subicular complex , 1991, The Journal of comparative neurology.

[27]  Larry R. Squire,et al.  Stereotaxic lesions of the hippocampus in monkeys: determination of surgical coordinates and analysis of lesions using magnetic resonance imaging , 1991, Journal of Neuroscience Methods.

[28]  S. Zola-Morgan,et al.  Hippocampal resections impair associative learning and recognition memory in the monkey , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  D. Amaral,et al.  The entorhinal cortex of the monkey: I. Cytoarchitectonic organization , 1987, The Journal of comparative neurology.

[30]  R. Desimone,et al.  A neural mechanism for working and recognition memory in inferior temporal cortex. , 1991, Science.

[31]  Lawrence Weiskrantz,et al.  The effects of fornix transection and combined fornix transection, mammillary body lesions and hippocampal ablations on object-pair association memory in the rhesus monkey , 1989, Behavioural Brain Research.

[32]  L. Squire,et al.  Damage to the perirhinal cortex exacerbates memory impairment following lesions to the hippocampal formation , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[33]  L R Squire,et al.  Lesions of the hippocampal formation but not lesions of the fornix or the mammillary nuclei produce long-lasting memory impairment in monkeys , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[34]  H. Harlow,et al.  A test-apparatus for monkeys , 1938 .

[35]  M. Mishkin,et al.  Monkeys with combined amygdalo-hippocampal lesions succeed in object discrimination learning despite 24-hour intertrial intervals. , 1984, Behavioral neuroscience.

[36]  M. Mishkin,et al.  Visual recognition in monkeys following rhinal cortical ablations combined with either amygdalectomy or hippocampectomy , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[37]  H. Eichenbaum,et al.  Complementary roles of the orbital prefrontal cortex and the perirhinal-entorhinal cortices in an odor-guided delayed-nonmatching-to-sample task. , 1992, Behavioral neuroscience.

[38]  M. Mishkin Memory in monkeys severely impaired by combined but not by separate removal of amygdala and hippocampus , 1978, Nature.

[39]  M. Mishkin,et al.  Effects on visual recognition of combined and separate ablations of the entorhinal and perirhinal cortex in rhesus monkeys , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[40]  W. Cowan,et al.  A stereotaxic atlas of the brain of the cynomolgus monkey (Macaca fascicularis) , 1984, The Journal of comparative neurology.

[41]  E. Murray,et al.  Monkeys (Macaca fascicularis) with rhinal cortex ablations succeed in object discrimination learning despite 24-hr intertrial intervals and fail at matching to sample despite double sample presentations. , 1992, Behavioral neuroscience.

[42]  L. Squire,et al.  The medial temporal lobe memory system , 1991, Science.

[43]  M. Mishkin,et al.  A selective mnemonic role for the hippocampus in monkeys: memory for the location of objects , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[44]  J. A. Horel,et al.  The performance of visual tasks while segments of the inferotemporal cortex are suppressed by cold , 1987, Behavioural Brain Research.

[45]  I. Riches,et al.  The effects of visual stimulation and memory on neurons of the hippocampal formation and the neighboring parahippocampal gyrus and inferior temporal cortex of the primate , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[46]  E. Murray Medial temporal lobe structures contributing to recognition memory: The amygdaloid complex versus the rhinal cortex. , 1992 .

[47]  L. Squire,et al.  Medial temporal lesions in monkeys impair memory on a variety of tasks sensitive to human amnesia. , 1985, Behavioral neuroscience.

[48]  S. Zeki Cortical projections from two prestriate areas in the monkey. , 1971, Brain research.

[49]  David P. Friedman,et al.  Cortical connections of the somatosensory fields of the lateral sulcus of macaques: Evidence for a corticolimbic pathway for touch , 1986, The Journal of comparative neurology.