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Cortical projections to anterior inferior temporal cortex in infant macaque monkeys

Published online by Cambridge University Press:  02 June 2009

Hillary R. Rodman  and
Michael J. Consuelos
Hillary R. Rodman
Affiliation:
Department of Psychology, Princeton University, Princeton
Michael J. Consuelos
Affiliation:
Department of Psychology, Princeton University, Princeton
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Abstract

Inferior temporal (IT) cortex is a “high-order” region of extrastriate visual cortex important for visual form perception and recognition in adult primates. The pattern of cortical afferents from both ipsilateral and contralateral hemispheres to anterior IT cortex was determined in infant macaque monkeys 7–18 weeks of age following injections of wheat-germ agglutinin-HRP. Within the ipsilateral hemisphere, the locations and laminar distribution of labeled cells were similar to those observed after comparable injections in adult monkeys. Specifically, ipsilateral afferents derived from visual areas V4, TEO, anterior and posterior IT, and STP, from parahippocampal, perirhinal, and parietal zones, and from several anterior zones including lateral and ventral frontal cortex, the insula, and cingulate cortex. Within the contralateral hemisphere, we observed labeled cells in homotopic regions of IT and in parahippocampal and perirhinal areas, as has been reported for adult monkeys. However, we also identified additional contralateral regions not previously known to provide input to anterior IT, including lateral and ventral frontal cortex, cingulate cortex, and STP. Overall, the strongest and most widespread projections from outside the temporal lobe were found in the youngest monkey, suggesting that some of these projections may represent transient circuitry necessary for the development of complex visual response properties in anterior IT.

Keywords

Visual cortex developmentCommissural pathwaysTransient connectionsInsulaCingulate cortexFrontal cortex
Type
Research Articles
Information
Visual Neuroscience , Volume 11 , Issue 1 , January 1994 , pp. 119 - 133
Copyright
Copyright © Cambridge University Press 1994

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References

Amaral, D.G., Insausti, R. & Cowan, W.M. (1987). The entorhinal cortex of the monkey: I. Cytoarchitectonic organization. Journal of Comparative Neurology 264, 326–355.CrossRefGoogle ScholarPubMed
Bachevalier, J., Brickson, M., Hagger, C. & Mishkin, M. (1990). Age and sex differences in the effects of selective temporal lobe lesion on the formation of visual discrimination habits in rhesus monkeys. Behavioral Neuroscience 104, 885–889.CrossRefGoogle ScholarPubMed
Bachevalier, J., Hagger, C. & Mishkin, M. (1991). Functional maturation of the occipitotemporal pathway in infant rhesus monkeys. In Brain Work and Mental Activity, ed. Lassen, N.A., Raichle, M.E. & Friberg, L., pp. 231–242. Copenhagen: Munksgaard.Google Scholar
Baleydier, C. & Maugiere, F. (1980). The duality of cingulate gyrus in monkey: Neuroanatomical study and functional hypothesis. Brain 103, 525–554.CrossRefGoogle ScholarPubMed
Barbas, H. (1988). Anatomic organization of basoventral and medio-dorsal visual recipient prefrontal regions in the rhesus monkey. Journal of Comparative Neurology 276, 313–342.CrossRefGoogle Scholar
Barbas, H. & Pandya, D.N. (1989). Architecture and intrinsic connections of the prefrontal cortex in the rhesus monkey. Journal of Comparative Neurology 286, 353–375.CrossRefGoogle ScholarPubMed
Baylis, G.C., Rolls, E.T. & Leonard, C.M. (1987). Functional subdivisions of the temporal lobe neocortex. Journal of Neuroscience 7, 330–342.CrossRefGoogle ScholarPubMed
Boussaoud, D., Desimone, R. & Ungerleider, L.G. (1991). Visual topography of area TEO in the macaque. Journal of Comparative Neurology 306, 554–575.CrossRefGoogle ScholarPubMed
Bruce, C.J., Desimone, R. & Gross, C.G. (1981). Visual properties of neurons in a polysensory area in the superior temporal sulcus of the macaque. Journal of Neurophysiology 46, 369–384.CrossRefGoogle Scholar
Demeter, S., Rosene, D.L. & Van Hoesen, G.W. (1990). Fields of origin and pathways of the interhemispheric commissures in temporal lobe of macaques. Journal of Comparative Neurology 302, 29–53.CrossRefGoogle ScholarPubMed
Desimone, R. & Gross, C.G. (1979). Visual areas in the temporal cortex of the macaque. Brain Research 178, 363–380.CrossRefGoogle ScholarPubMed
Desimone, R., Fleming, J. & Gross, C.G. (1980). Prestriate afferents to inferior temporal cortex: An HRP study. Brain Research 184, 41–55.CrossRefGoogle ScholarPubMed
Desimone, R. & Ungerleider, L.G. (1989). Neural mechanisms of visual perception in monkeys. In Handbook of Neuropsychology, Vol. II, ed. Boller, R. & Grafman, J., pp. 267–299. Amsterdam: Elsevier.Google Scholar
Felleman, D.J. & Van Essen, D.C. (1991). Distributed hierarchical processing in primate cerebral cortex. Cerebral Cortex 1, 1–48.CrossRefGoogle ScholarPubMed
Fenstemaker, S.B. (1986). The organization and connections of visual cortical area TEO in the macaque. Unpublished doctoral dissertation, Princeton University, Princeton, New Jersey.Google Scholar
Fenstemaker, S.B., Albright, T.D. & Gross, C.G. (1985). Organization and neuronal properties of visual area TEO. Society for Neuroscience Abstracts 11, 1012.Google Scholar
Fenstemaker, S.B., Olson, C.R. & Gross, C.G. (1984). Afferent connections of macaque visual areas V4 and TEO. Association for Research in Vision and Ophthalmology Abstracts 25, 279.Google Scholar
Fuster, J.M., Bauer, R.H. & Jervey, J.P. (1985). Functional interactions between inferotemporal and prefrontal cortex in a cognitive task. Brain Research 330, 229–307.CrossRefGoogle Scholar
Gattass, R.G., Sousa, A.P.B. & Gross, C.G. (1988). Visuotopic organization and extent of V3 and V4 of the macaque. Journal of Neuroscience 8, 1831–1845.CrossRefGoogle ScholarPubMed
Goldman-Rakic, P.S. (1987). Circuitry of primate prefrontal cortex and regulation of behavior by representational memory. In Handbook of Physiology: The Nervous System, Vol. 5, pp. 373–417. Bethesda, Maryland: American Physiological Society.Google Scholar
Gross, C.G. (1992). Representation of visual stimuli in inferior temporal cortex. Philosophical Transactions of the Royal Society B (London) 335, 3–10.Google ScholarPubMed
Gross, C.G. & Mishkin, M. (1977). The neural basis of stimulus equivalence across retinal translation. In Lateralization in the Nervous System, ed. Harnad, S., Doty, R., Jaynes, J., Goldstein, L. & Krauthamer, G., pp. 109–122. New York: Academic Press.CrossRefGoogle Scholar
Gross, C.G., Rodman, H.R., Gochin, P.M. & Colombo, M.W. (1993). Inferior temporal cortex as a pattern recognition device. In Proceedings of the Third Annual NEC Res. Symposium, ed. Baum, E., pp. 44–73. Philadelphia: Siam.Google Scholar
Gross, C.G. & Weiskrantz, L. (1962). Some changes in behavior produced by lateral frontal lesions in the macaque. In The Frontal Granular Cortex and Behavior, ed. Warren, J.M. & Akert, K., pp. 74–98. New York: McGraw-Hill.Google Scholar
Hagger, C., Brickson, M. & Bachevalier, J. (1985). Sparing of visual recognition after neonatal lesions of inferior temporal cortex in infant rhesus monkeys. Society for Neuroscience Abstracts 11, 831.Google Scholar
Iwai, E. & Yukie, M. (1987). Amygdalofugal and amygdalopetal connections with modality-specific visual cortical areas in macaques (Macacafuscata, M. mulatto, and M. fascicularis). Journal of Comparative Neurology 261, 382–387.Google Scholar
Jouandet, M.L. & Gazzaniga, M.S. (1979). Cortical field of origin of the anterior commissure of the rhesus monkey. Experimental Neurology 66, 381–397.CrossRefGoogle ScholarPubMed
Kennedy, H., Bullier, J. & Dehay, C. (1989). Transient projection from the superior temporal sulcus to area 17 in the newborn macaque monkey. Proceedings of the National Academy of Sciences of the U.S.A. 86, 8093–8097.CrossRefGoogle ScholarPubMed
LaMantia, A.S. & Rakic, P. (1984). The number, size, myelination, and regional variation of axons in the corpus callosum and anterior commissure of the developing rhesus monkey. Society for Neuroscience Abstracts 10, 1081.Google Scholar
LaMantia, A.S. & Rakic, P. (1990). Axon overproduction and elimination in the corpus callosum of the developing rhesus monkey. Journal of Neuroscience 10, 2156–2175.CrossRefGoogle ScholarPubMed
Marttn-Elkins, C.L. & Horel, J.A. (1992). Cortical afferents to behaviorally defined regions of the inferior temporal and parahippocampal gyri as demonstrated by WGA-HRP. Journal of Comparative Neurology 321, 177–192.CrossRefGoogle Scholar
Mesulam, M.-M. (1982). Principles of horseradish peroxidase neuro-histochemistry and their applications for tracing neural pathways: Axonal transport, enzyme histochemistry and light-microscopic analysis. In Tracing Neural Connections with Horseradish Peroxidase, ed. Mesulam, M.-M., Chichester, New York: Wiley & Co.Google Scholar
Mesulam, M.-M. & Mufson, E.J. (1982). Insula of the Old World monkey: I. Architectonics in the insulo-orbito-temporal component of the paralimbic brain. Journal of Comparative Neurology 212, 1–22.CrossRefGoogle ScholarPubMed
Morel, A. & Bullier, J. (1990). Anatomical segregation of two cortical visual pathways in the macaque monkey. Visual Neuroscience 4, 555–578.CrossRefGoogle ScholarPubMed
Mufson, E.J. & Mesulam, M.-M. (1982). Insula of the Old World monkey: II. Afferent cortical input and comments on the claustrum. Journal of Comparative Neurology 212, 23–27.CrossRefGoogle ScholarPubMed
Rocha-Miranda, C.E., Bender, D.B., Gross, C.G. & Mishkin, M. (1975). Visual activation of neurons in inferotemporal cortex depends on striate cortex and forebrain commissures. Journal of Neurophysiology 38, 475–491.CrossRefGoogle ScholarPubMed
Rodman, H.R. (1991). Methods for repeated recording in visual cortex of anesthetized and awake behaving infant monkeys. Journal of Neuroscience Methods 38, 209–222.CrossRefGoogle ScholarPubMed
Rodman, H.R., Consuelos, M.J. & Gross, C.G. (1990). Cortical afferents to inferior temporal cortex in infant macaque monkeys. Association for Research in Vision and Ophthalmology Abstracts 31, 399.Google Scholar
Rodman, H.R., Nace, K.L., Woods, T.M., Gross, C.G. & Rebmann, N.S. (1993 a) Transient inputs to inferior temporal cortex in infant macaques. Society for Neuroscience Abstracts 19, 972.Google Scholar
Rodman, H.R., Ó Scalaidhe, S.P. & Gross, C.G. (1993 b). Visual response properties of neurons in temporal cortical visual areas of infant monkeys. Journal of Neurophysiology 70, 1115–1136.CrossRefGoogle ScholarPubMed
Rodman, H.R., Skelly, J.P. & Gross, C.G. (1991). Stimulus selectivity and state dependence of activity in inferior temporal cortex of infant monkeys. Proceedings of the National Academy of Sciences of the U.S.A. 88, 7572–7575.CrossRefGoogle ScholarPubMed
Seltzer, B. & Pandya, D.N. (1978). Afferent cortical connections and architectonics of the superior temporal sulcus and surrounding cortex in the rhesus monkey. Brain Research 149, 11–24.CrossRefGoogle ScholarPubMed
Seltzer, B. & Pandya, D.N. (1989). Frontal lobe connections of the superior temporal sulcus in the rhesus monkey. Journal of Comparative Neurology 281, 97–113.CrossRefGoogle ScholarPubMed
Shiwa, T. (1987). Corticocortical projections to the monkey temporal lobe with particular reference to the visual processing pathways. Archives Italiennes de Biologie 125, 139–154.Google Scholar
Ungerleider, L.G., Gaffan, D. & Pelak, V.S. (1989). Projections from inferior temporal cortex to prefrontal cortex via the uncinate fascicle in rhesus monkeys. Experimental Brain Research 76, 473–484.CrossRefGoogle ScholarPubMed
Vogt, B.A. & Pandya, D.N. (1987). Cingulate cortex of the rhesus monkey. II. Cortical afferents. Journal of Comparative Neurology 262, 271–289.CrossRefGoogle ScholarPubMed
Vogt, B.A., Pandya, D.N. & Rosene, D.L. (1987). Cingulate cortex of the rhesus monkey. I. Cytoarchitecture and thalamic afferents. Journal of Comparative Neurology 262, 256–270.CrossRefGoogle ScholarPubMed
von Bonin, G. & Bailey, P. (1947). The Neocortex of Macaca mulatto. Urbana, Illinois: University of Illinois Press.Google Scholar
Walker, A.E. (1940). A cytoarchitectural study of the prefrontal area of the macaque monkey. Journal of Comparative Neurology 73, 58–86.Google Scholar
Webster, M.J., Ungerleider, L.G. & Bachevalier, J. (1991). Connections of inferior temporal areas TE and TEO with medial temporal-lobe structures in infant and adult monkeys. Journal of Neuroscience 11, 1095–1116.CrossRefGoogle ScholarPubMed
Weller, R.E. & Kaas, J.H. (1987). Subdivisions and connections of inferior temporal cortex in owl monkeys. Journal of Comparative Neurology 256, 137–172.CrossRefGoogle ScholarPubMed
Weller, R.E. & Steele, G.E. (1992). Cortical connections of subdivisions of inferior temporal cortex in squirrel monkeys. Journal of Comparative Neurology 324, 37–66.CrossRefGoogle ScholarPubMed
Wilson, F.A.W., Ó Scalaidhe, S.P. & Goldman-Rakic, P.S. (1993). Dissociation of object and spatial processing domains in primate prefrontal cortex. Science 260, 1955–1958.CrossRefGoogle ScholarPubMed
Yukie, M. & Iwai, E. (1988). Direct projection from ventral TE area of the inferotemporal cortex to hippocampal field CA1 in the monkey. Neuroscience Letters 88, 6–10.CrossRefGoogle ScholarPubMed
Zeki, S.M. (1973). Comparison of the cortical degeneration in the visual regions of the temporal lobe of the monkey following section of the anterior commissure and the splenium. Journal of Comparative Neurology 148, 167–176.CrossRefGoogle ScholarPubMed