Cortical afferents to behaviorally defined regions of the inferior temporal and parahippocampal gyri as demonstrated by WGA‐HRP

The inferior temporal gyrus in the monkey appears to be unique among the many extrastriate visual cortices in its importance for normal performance of delayed match‐to‐sample, a visual memory task. However, the anatomical pathway providing visual information to this portion of the temporal lobe remains unclear. In this study, wheat germ agglutinin conjugated to horseradish peroxidase (WGA‐HRP) was injected into the anterior inferior temporal gyrus and heavy projections were found to arise in cytoarchitectural area TF of the parahippocampal gyrus, as well as moderate projections in more posterior portions of inferior temporal gyrus and perirhinal and entorhinal cortices. Subsequently, WGA‐HRP was injected into area TF, resulting in retrogradely labeled cells primarily located in the portions of area TF adjacent to the injection and also in the occipitotemporal sulcus including the ventral portion of the prestriate visual area V4. Moderate projections were found to originate from the dorsal region of area V4 in the lunate sulcus, portions of the caudal parietal lobe, the posterior bank of caudal superior temporal sulcus, and area OPT located at the tip of the superior temporal sulcus. The middle temporal gyrus, foveal prestriate cortex, and area TEO, a transitional area between temporal and occipital visual areas, were all free from retrogradely labeled cells. These latter areas are included in the well‐established anatomical system that is known to carry visual information from striate cortex through prestriate to eventually reach dorsal portions of inferotemporal cortex which is coincident with the temporal lobe visual area TE. It is suggested here that there is an additional ventral pathway into area TE as well, which includes projections through portions of the prestriate cortex, occipitotemporal sulcus, and parahippocampal gyrus, ultimately reaching the anterior inferior temporal gyrus, an area that may be specialized to hold visual information over brief periods of time. © 1992 Wiley‐Liss, Inc.

[1]  H. Klüver,et al.  An analysis of certain effects of bilateral temporal lobectomy in the rhesus monkey, with special reference to "psychic blindness." , 1938 .

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

[3]  G. Bonin,et al.  The neocortex of Macaca mulatta , 1947 .

[4]  K. Chow Further studies on selective ablation of associative cortex in relation to visually mediated behavior. , 1952, Journal of comparative and physiological psychology.

[5]  K. Pribram,et al.  Visual discrimination performance following partial ablations of the temporal lobe. I. Ventral vs. lateral. , 1954, Journal of comparative and physiological psychology.

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

[7]  M. Mishkin,et al.  OCCIPITOTEMPORAL CORTICOCORTICAL CONNECTIONS IN THE RHESUS MONKEY. , 1965, Experimental neurology.

[8]  S. Zeki,et al.  The secondary visual areas of the monkey. , 1969, Brain research.

[9]  D. Benson,et al.  Visual form agnosia. A specific defect in visual discrimination. , 1969, Archives of neurology.

[10]  B. Cragg The topography of the afferent projections in the circumstriate visual cortex of the monkey studied by the Nauta method. , 1969, Vision research.

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

[12]  D. Benson,et al.  Associative visual agnosia. , 1971, Archives of neurology.

[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]  S. Iversen Visual discrimination deficits associated with posterior inferotemporal lesions in the monkey. , 1973, Brain research.

[15]  P. Dean The effect of inferotemporal lesions on memory for visual stimuli in rhesus monkeys. , 1974, Brain research.

[16]  M. Albert,et al.  Visual agnosia-prosopagnosia. A clinicopathologic correlation. , 1974, Archives of neurology.

[17]  Deepak N. Pandya,et al.  Some connections of the entorhinal (area 28) and perirhinal (area 35) cortices of the rhesus monkey. III. Efferent connections , 1975, Brain Research.

[18]  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.

[19]  P. Dean Effects of inferotemporal lesions on the behavior of monkeys. , 1976, Psychological bulletin.

[20]  B. Vogt,et al.  Retrosplenial cortex in the rhesus monkey: A cytoarchitectonic and golgi study , 1976, The Journal of comparative neurology.

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

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

[23]  D. C. Essen,et al.  The topographic organization of rhesus monkey prestriate cortex. , 1978, The Journal of physiology.

[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]  S. Zeki,et al.  The cortical projections of foveal striate cortex in the rhesus monkey. , 1978, The Journal of physiology.

[26]  Arjun Sahgal,et al.  Categorization and retrieval after selective inferotemporal lesions in monkeys , 1978, Brain Research.

[27]  Arjun Sahgal,et al.  The effects of foveal prestriate and inferotemporal lesions on matching to sample behaviour in monkeys , 1978, Neuropsychologia.

[28]  D. Crowne,et al.  Effects of anterior and posterior inferotemporal lesions on discrimination reversal in the monkey , 1979, Neuropsychologia.

[29]  G. Handelmann,et al.  Hippocampus, space, and memory , 1979 .

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

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

[32]  E. Iwai,et al.  The locus of the posterior subdivision of the inferotemporal visual learning area in the monkey , 1980, Brain Research.

[33]  R. Desimone,et al.  Prestriate afferents to inferior temporal cortex: an HRP study , 1980, Brain Research.

[34]  M Mishkin,et al.  Organization of the amygdalopetal projections from modality‐specific cortical association areas in the monkey , 1980, The Journal of comparative neurology.

[35]  D. Pandya,et al.  Converging visual and somatic sensory cortical input to the intraparietal sulcus of the rhesus monkey , 1980, Brain Research.

[36]  Organization of Extrastriate Visual Areas in the Macaque Monkey , 1981 .

[37]  J. A. Horel,et al.  Behavioral effect of local cooling in temporal lobe of monkeys. , 1982, Journal of neurophysiology.

[38]  D. Pandya,et al.  Intrinsic connections and architectonics of posterior parietal cortex in the rhesus monkey , 1982, The Journal of comparative neurology.

[39]  M. Mishkin A memory system in the monkey. , 1982, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[40]  W. Maguire,et al.  Visuotopic organization of the prelunate gyrus in rhesus monkey , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[41]  D. Amaral,et al.  Amygdalo‐cortical projections in the monkey (Macaca fascicularis) , 1984, The Journal of comparative neurology.

[42]  J. A. Horel Cold lesions in inferotemporal cortex produce reversible deficits in learning and retention of visual discriminations , 1984 .

[43]  J. A. Horel,et al.  Visual learning suppressed by cooling the temporal pole. , 1984, Behavioral neuroscience.

[44]  G. V. Van Hoesen,et al.  Multimodal amnesic syndrome following bilateral temporal and basal forebrain damage. , 1985, Archives of neurology.

[45]  M. Voytko Visual learning and retention examined with reversible cold lesions of the anterior temporal lobe , 1986, Behavioural Brain Research.

[46]  Leslie G. Ungerleider,et al.  Cortical connections of visual area MT in the macaque , 1986, The Journal of comparative neurology.

[47]  D. J. Felleman,et al.  Anatomical and physiological asymmetries related to visual areas V3 and VP in macaque extrastriate cortex , 1986, Vision Research.

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

[49]  M. W. Brown,et al.  Neuronal evidence that inferomedial temporal cortex is more important than hippocampus in certain processes underlying recognition memory , 1987, Brain Research.

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

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

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

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

[54]  C. Gross,et al.  Visuotopic organization and extent of V3 and V4 of the macaque , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[55]  J. A. Horel,et al.  Reversible cold lesions of the parahippocampal gyrus in monkeys result in deficits on the delayed match-to-sample and other visual tasks , 1989, Behavioural Brain Research.

[56]  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.

[57]  J. A. Horel,et al.  Retention deficits produced in monkeys with reversible cold lesions in the prestriate cortex , 1989, Behavioural Brain Research.