Perirhinal and parahippocampal cortices of the macaque monkey: Cortical afferents

Neuropsychological studies have recently demonstrated that the macaque monkey perirhinal (areas 35 and 36) and parahippocampal (areas TH and TF) cortices contribute importantly to normal memory function. Unfortunately, neuroanatomical information concerning the cytoarchitectonic organization and extrinsic connectivity of these cortical regions is meager. We investigated the organization of cortical inputs to the macaque monkey perirhinal and parahippocampal cortices by placing discrete injections of the retrograde tracers fast blue, diamidino yellow, and wheat germ agglutinin conjugated to horseradish peroxidase throughout these areas. We found that the macaque monkey perirhinal and parahippocampal cortices receive different complements of cortical inputs. The major cortical inputs to the perirhinal cortex arise from the unimodal visual areas TE and rostral TEO and from area TF of the parahippocampal cortex. The perirhinal cortex also receives projections from the dysgranular and granular subdivisions of the insular cortex and from area 13 of the orbitofrontal cortex. In contrast, area TF of the parahippocampal cortex receives its strongest input from more caudal visual areas V4, TEO, and caudal TE, as well as prominent inputs from polymodal association cortices, including the retrosplenial cortex and the dorsal bank of the superior temporal sulcus. Area TF also receives projections from areas 7a and LIP of the posterior parietal lobe, insular cortex, and areas 46, 13, 45, and 9 of the frontal lobe. As with area TF, area TH receives substantial projections from the retrosplenial cortex as well as moderate projections from the dorsal bank of the superior temporal sulcus; unlike area TF, area TH receives almost no innervation from areas TE and TEO. It does, however, receive relatively strong inputs from auditory association areas TE and TEO. It does, however, receive relatively strong inputs from auditory association areas on the convexity of the superior temporal gyrus. © 1994 Wiley‐Liss, Inc.

[1]  Jelliffe Vergleichende Lokalisationslehre der Grosshirnrinde , 1910 .

[2]  A. Walker,et al.  A cytoarchitectural study of the prefrontal area of the macaque monkey , 1940 .

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

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

[5]  G. Ettlinger,et al.  Somaesthetic Alternation, Discrimination and Orientation after Frontal and Parietal Lesions in Monkeys , 1958 .

[6]  G. Ettlinger,et al.  Posterior biparietal ablations in the monkey. Changes to neurological and behavioral testing. , 1960, Archives of neurology.

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

[8]  M Hallett,et al.  Intra- and interhemispheric connections of the neocortical auditory system in the rhesus monkey. , 1969, Brain research.

[9]  D. Pandya,et al.  Cortico-cortical connections in the rhesus monkey. , 1969, Brain research.

[10]  T. Powell,et al.  An anatomical study of converging sensory pathways within the cerebral cortex of the monkey. , 1970, Brain : a journal of neurology.

[11]  D. Pandya,et al.  Efferent cortico-cortical projections of the prefrontal cortex in the rhesus monkey. , 1971, Brain research.

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

[13]  W. Pohl,et al.  Dissociation of spatial discrimination deficits following frontal and parietal lesions in monkeys. , 1973, Journal of comparative and physiological psychology.

[14]  M. Merzenich,et al.  Representation of the cochlear partition of the superior temporal plane of the macaque monkey. , 1973, Brain research.

[15]  D. Pandya,et al.  Some connections of the entorhinal (area 28) and perirhinal (area 35) cortices of the rhesus monkey. I. Temporal lobe afferents , 1975, Brain Research.

[16]  Deepak N. Pandya,et al.  Some connections of the entorhinal (area 28) and perirhinal (area 35) cortices of the rhesus monkey. II. Frontal lobe afferents , 1975, Brain Research.

[17]  H. Burton,et al.  Areal differences in the laminar distribution of thalamic afferents in cortical fields of the insular, parietal and temporal regions of primates , 1976, The Journal of comparative neurology.

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

[19]  D. Pandya,et al.  Limbic and sensory connections of the inferior parietal lobule (area PG) in the rhesus monkey: A study with a new method for horseradish peroxidase histochemistry , 1977, Brain Research.

[20]  A. Milner,et al.  Visuo-Spatial Performance Following Posterior Parietal and Lateral Frontal Lesions in Stumptail Macaques , 1977, Cortex.

[21]  Leslie G. Ungerleider,et al.  Extrapersonal spatial orientation: The role of posterior parietal, anterior frontal, and inferotemporal cortex , 1977, Experimental Neurology.

[22]  G. Ettlinger,et al.  Disturbance of Cage-Finding in the Monkey , 1978, Cortex.

[23]  K. Pribram,et al.  The role of frontal and parietal cortex in cognitive processing: tests of spatial and sequence functions. , 1978, Brain : a journal of neurology.

[24]  D. Pandya,et al.  Afferent cortical connections and architectonics of the superior temporal sulcus and surrounding cortex in the rhesus monkey , 1978, Brain Research.

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

[26]  K. Rockland,et al.  Laminar origins and terminations of cortical connections of the occipital lobe in the rhesus monkey , 1979, Brain Research.

[27]  Michael Petrides,et al.  Restricted posterior parietal lesions in the rhesus monkey and performance on visuospatial tasks , 1979, Brain Research.

[28]  R. Desimone,et al.  Visual areas in the temporal cortex of the macaque , 1979, Brain Research.

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

[30]  F Mauguiere,et al.  The duality of the cingulate gyrus in monkey. Neuroanatomical study and functional hypothesis. , 1980, Brain : a journal of neurology.

[31]  R. Desimone,et al.  Visual properties of neurons in a polysensory area in superior temporal sulcus of the macaque. , 1981, Journal of neurophysiology.

[32]  Visual mechanisms in the temporal and prestriate association cortices of the monkey , 1981 .

[33]  R. Morris,et al.  Place navigation impaired in rats with hippocampal lesions , 1982, Nature.

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

[35]  M. Mesulam,et al.  Insula of the old world monkey. II: Afferent cortical input and comments on the claustrum , 1982, The Journal of comparative neurology.

[36]  H. Kuypers,et al.  Collaterals of rubrospinal neurons to the cerebellum in rat. A retrograde fluorescent double labeling study , 1983, Brain Research.

[37]  D. Amaral,et al.  An air pressure system for the injection of tracer substances into the brain , 1983, Journal of Neuroscience Methods.

[38]  P. Goldman-Rakic,et al.  Dual pathways connecting the dorsolateral prefrontal cortex with the hippocampal formation and parahippocampal cortex in the rhesus monkey , 1984, Neuroscience.

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

[40]  H. Kuypers,et al.  Fluorescent Neuronal Tracers , 1984 .

[41]  S. Corkin Lasting Consequences of Bilateral Medial Temporal Lobectomy: Clinical Course and Experimental Findings in H.M. , 1984 .

[42]  M. Mesulam,et al.  Cortical afferent input to the principals region of the rhesus monkey , 1985, Neuroscience.

[43]  Ellen Covey,et al.  Cortical Visual Areas of the Macaque: Possible Substrates for Pattern Recognition Mechanisms , 1985 .

[44]  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.

[45]  L. Squire,et al.  Korsakoff's syndrome: a study of the relation between anterograde amnesia and remote memory impairment. , 1986, Behavioral neuroscience.

[46]  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.

[47]  H. Groenewegen,et al.  Connections of the parahippocampal cortex. I. Cortical afferents , 1986, The Journal of comparative neurology.

[48]  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.

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

[50]  R E Weller,et al.  Subdivisions and connections of inferior temporal cortex in owl monkeys , 1987, The Journal of comparative neurology.

[51]  M. Yukie,et al.  Amygdalofugal and amygdalopetal connections with modality‐specific visual cortical areas in macaques (macaca fuscata, M. mulatta, and M. fascicularis) , 1987, The Journal of comparative neurology.

[52]  E. Rolls,et al.  Functional subdivisions of the temporal lobe neocortex , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[54]  D. Pandya,et al.  Cingulate cortex of the rhesus monkey: II. Cortical afferents , 1987, The Journal of comparative neurology.

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

[56]  A. Sirigu,et al.  Pure Topographical Disorientation: A Definition and Anatomical Basis , 1987, Cortex.

[57]  P. Goldman-Rakic,et al.  Common cortical and subcortical targets of the dorsolateral prefrontal and posterior parietal cortices in the rhesus monkey: evidence for a distributed neural network subserving spatially guided behavior , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[59]  R. Sutherland,et al.  Contributions of cingulate cortex to two forms of spatial learning and memory , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[60]  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.

[61]  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.

[62]  R. Andersen Visual and eye movement functions of the posterior parietal cortex. , 1989, Annual review of neuroscience.

[63]  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.

[64]  P. Goldman-Rakic,et al.  Posterior parietal cortex in rhesus monkey: I. Parcellation of areas based on distinctive limbic and sensory corticocortical connections , 1989, The Journal of comparative neurology.

[65]  R. M. Siegel,et al.  Corticocortical connections of anatomically and physiologically defined subdivisions within the inferior parietal lobule , 1990, The Journal of comparative neurology.

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

[67]  R. Andersen,et al.  Visual receptive field organization and cortico‐cortical connections of the lateral intraparietal area (area LIP) in the macaque , 1990, The Journal of comparative neurology.

[68]  D. C. Essen,et al.  Modular and hierarchical organization of extrastriate visual cortex in the macaque monkey. , 1990, Cold Spring Harbor symposia on quantitative biology.

[69]  Leslie G. Ungerleider,et al.  Visual topography of area TEO in the macaque , 1991, The Journal of comparative neurology.

[70]  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.

[71]  R E Weller,et al.  Cortical connections of the caudal subdivision of the dorsolateral area (V4) in monkeys , 1991, The Journal of comparative neurology.

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

[73]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[74]  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.

[75]  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 .

[76]  C. Geula,et al.  Cytoarchitecture and neural afferents of orbitofrontal cortex in the brain of the monkey , 1992, The Journal of comparative neurology.

[77]  R. Weller,et al.  Cortical connections of subdivisions of inferior temporal cortex in squirrel monkeys , 1992, The Journal of comparative neurology.

[78]  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.

[79]  C R Olson,et al.  Posterior cingulate cortex: sensory and oculomotor properties of single neurons in behaving cat. , 1992, Cerebral cortex.

[80]  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.

[81]  D. Pandya,et al.  Efferent cortical connections of multimodal cortex of the superior temporal sulcus in the rhesus monkey , 1992, The Journal of comparative neurology.

[82]  J. A. Horel,et al.  Cortical afferents to behaviorally defined regions of the inferior temporal and parahippocampal gyri as demonstrated by WGA‐HRP , 1992, The Journal of comparative neurology.

[83]  C R Olson,et al.  Topographic organization of cortical and subcortical projections to posterior cingulate cortex in the cat: Evidence for somatic, ocular, and complex subregions , 1992, The Journal of comparative neurology.

[84]  P. Goldman-Rakic,et al.  Dissociation of object and spatial processing domains in primate prefrontal cortex. , 1993, Science.

[85]  M. Mishkin,et al.  Hippocampectomized monkeys can remember one place but not two , 1993, Neuropsychologia.

[86]  L. Squire,et al.  Neuroanatomy of memory. , 1993, Annual review of neuroscience.

[87]  D. Amaral,et al.  Lesions of the perirhinal and parahippocampal cortices in the monkey produce long-lasting memory impairment in the visual and tactual modalities , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[88]  David P. Friedman,et al.  A modality-specific somatosensory area within the insula of the rhesus monkey , 1993, Brain Research.

[89]  R. Desimone,et al.  Activity of neurons in anterior inferior temporal cortex during a short- term memory task , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[90]  L. Jarrard On the role of the hippocampus in learning and memory in the rat. , 1993, Behavioral and neural biology.

[91]  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.

[92]  Leslie G. Ungerleider,et al.  Cortical connections of inferior temporal area TEO in macaque monkeys , 1993, The Journal of comparative neurology.

[93]  W. Suzuki,et al.  Topographic organization of the reciprocal connections between the monkey entorhinal cortex and the perirhinal and parahippocampal cortices , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[94]  D. Mumby,et al.  Rhinal cortex lesions and object recognition in rats. , 1994, Behavioral neuroscience.