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Comparison of subcortical connections of inferior temporal and posterior parietal cortex in monkeys

Published online by Cambridge University Press:  02 June 2009

Joan S. Baizer
Affiliation:
Laboratory of Neuropsychology, National Institute of Mental Health, Bethesda
Robert Desimone
Affiliation:
Laboratory of Neuropsychology, National Institute of Mental Health, Bethesda
Leslie G. Ungerleider
Affiliation:
Laboratory of Neuropsychology, National Institute of Mental Health, Bethesda

Abstract

To investigate the subcortical connections of the object vision and spatial vision cortical processing pathways, we injected the inferior temporal and posterior parietal cortex of six Rhesus monkeys with retrograde or anterograde tracers. The temporal injections included area TE on the lateral surface of the hemisphere and adjacent portions of area TEO. The parietal injections covered the posterior bank of the intraparietal sulcus, including areas VIP and LIP. Our results indicate that several structures project to both the temporal and parietal cortex, including the medial and lateral pulvinar, claustrum, and nucleus basalis. However, the cells in both the pulvinar and claustrum that project to the two systems are mainly located in different parts of those structures, as are the terminals which arise from the temporal and parietal cortex. Likewise, the projections from the temporal and parietal cortex to the caudate nucleus and putamen are largely segregated. Finally, we found projections to the pons and superior colliculus from parietal but not temporal cortex, whereas we found the lateral basal and medial basal nuclei of the amygdala to be reciprocally connected with temporal but not parietal cortex. Thus, the results show that, like the cortical connections of the two visual processing systems, the subcortical connections are remarkably segregated.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1993

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References

Aggleton, J.P., Burton, M.J. & Passingham, R.E. (1980). Cortical and subcortical afferents to the amygdala of the rhesus monkey (Macaca mulatta). Brain Research 190, 347368.CrossRefGoogle Scholar
Amaral, D.G. & Price, J.L. (1984). Amygdalo-cortical projections in the monkey (Macaca fascicularis). Journal of Comparative Neurology 230, 465496.CrossRefGoogle ScholarPubMed
Asanuma, C., Andersen, R.A. & Cowan, W.M. (1985). The thalamic relations of the caudal inferior parietal lobule and the lateral prefrontal cortex in monkeys: Divergent cortical projections from cell clusters in the medial pulvinar nucleus. Journal of Comparative Neurology 241, 357381.CrossRefGoogle ScholarPubMed
Baizer, J.S., Ungerleider, L.G. & Desimone, R. (1991 a). Organization of visual inputs to inferior temporal and posterior parietal cortex in macaques. Journal of Neuroscience 11, 168190.CrossRefGoogle ScholarPubMed
Baizer, J.S., Ungerleider, L.G. & Desimone, R. (1991 b). Subcortical connections of inferior temporal and posterior parietal cortex in macaques. Society for Neuroscience Abstracts 17, 845.Google Scholar
Baleydier, C. & Mauguière, F. (1977). Pulvinar-lateral posterior afferents to cortical area 7 in monkeys demonstrated by horseradish peroxidase tracing technique. Experimental Brain Research 27, 501507.CrossRefGoogle Scholar
Baleydier, C. & Morel, A. (1992). Segregated thalamocortical pathways to inferior parietal and inferotemporal cortex in macaque monkey. Visual Neuroscience 8, 391405.CrossRefGoogle ScholarPubMed
Bender, D.B. (1981). Retinotopic organization of macaque pulvinar. Journal of Neurophysiology 46, 672693.CrossRefGoogle ScholarPubMed
Benevento, L.A. & Davis, P. (1977). Topographical projections of the prestriate cortex to the pulvinar nuclei in the macaque monkey: An autoradiographic study. Experimental Brain Research 30, 405424.Google Scholar
Benevento, L.A. & Fallon, J.H. (1975). The ascending projections of the superior colliculus in the rhesus monkey (Macaca mulatta). Journal of Comparative Neurology 160, 339362.CrossRefGoogle ScholarPubMed
Benevento, L.A. & Miller, J. (1981). Visual responses of single neurons in the caudal lateral pulvinar of the macaque monkey. Journal of Neuroscience 11, 12681278.CrossRefGoogle Scholar
Benevento, L.A. & Rezak, M. (1976). The cortical projections of the inferior pulvinar and adjacent lateral pulvinar in the rhesus monkey (Macaca mulatta): An autoradiographic study. Brain Research 108, 124.CrossRefGoogle ScholarPubMed
Benevento, L.A. & Standage, G.P. (1983). The organization of projections of the retino-recipient and nonretino-recipient nuclei of the pretectal complex and layers of the superior colliculus to the lateral pulvinar and the medial pulvinar in the rhesus monkey. Journal of Comparative Neurology 218, 307336.CrossRefGoogle Scholar
Bonin, G., Von Bailey, P. (1947). The Neocortex of Macaca mulatta. Urbana, Illinois: University of Illinois Press.Google Scholar
Boussaoud, D., Desimone, R. & Ungerleider, L.G. (1991). Visual topography of area TEO in the macaque. Journal of Comparative Neurology 306, 554575.CrossRefGoogle ScholarPubMed
Boussaoud, D., Desimone, R. & Ungerleider, L.G. (1992). Subcortical connections of MST and FST in the macaque. Visual Neuroscience 9, 291302.CrossRefGoogle Scholar
Brodal, P. (1978). The corticopontine projection in the rhesus monkey. Origin and principles of organization. Brain 101, 251283.CrossRefGoogle ScholarPubMed
Campos-Ortega, J.A. & Hayhow, W.R. (1972). On the organisation of the visual cortical projection to the pulvinar in Macaca mulatta. Brain, Behavior, and Evolution 6, 394423.CrossRefGoogle Scholar
Cavada, C. & Goldman-Rakic, P.S. (1989). Posterior parietal cortex in rhesus monkey: I. Parcellation of areas based on distinctive limbic and sensory corticocortical connections. Journal of Comparative Neurology 287, 393421.CrossRefGoogle ScholarPubMed
Cavada, C. & Goldman-Rakic, P.S. (1991). Topographic segregation of corticostriatal projections from posterior parietal subdivisions in the macaque monkey. Neuroscience 42, 683696.CrossRefGoogle ScholarPubMed
Colby, C.L. & Olson, C.R. (1985). Visual topography of cortical projections to monkey superior colliculus. Society for Neuroscience Abstracts 11, 1244.Google Scholar
Cowan, W.M., Gottleib, D.I., Hendrickson, A.E., Price, J.L. & Woolsey, T.A. (1972). The autoradiographic demonstration of axonal connections in the central nervous system. Brain Research 37, 2151.CrossRefGoogle ScholarPubMed
Desimone, R. & Gross, C.G. (1979). Visual areas in the superior temporal cortex of the macaque. Brain Research 178, 363380.CrossRefGoogle Scholar
Desimone, R. & Ungerleider, L.G. (1989). Neural mechanisms of visual processing in monkeys. In Handbook of Neuropsychology, ed. Boller, F. & Grafman, J., pp. 267299. Amsterdam: Elsevier.Google Scholar
Divac, I., Vail, J.H.La, Rakic, P. & Winston, K.R. (1977). Heterogeneous afferents to the inferior parietal lobule of the rhesus monkey revealed by the retrograde transport method. Brain Research 123, 197207.CrossRefGoogle Scholar
Felleman, D.J. & Van Essen, D.C. (1991). Distributed hierarchical processing in the primate cerebral cortex. Cerebral Cortex 1, 147.CrossRefGoogle ScholarPubMed
Friedman, D.P., Li, L. & Ungerleider, L.G. (1989). Origins of thalamic projections to layer I of the cerebral cortex of the monkey. Society for Neuroscience Abstracts 15, 311.Google Scholar
Fries, W. (1984). Cortical projections to the superior colliculus in the macaque monkey: A retrograde study using horseradish peroxidase. Journal of Comparative Neurology 230, 5576.CrossRefGoogle Scholar
Gaffan, D. & Harrison, S. (1987). Amygdalectomy and disconnection in visual learning for auditory secondary reinforcement by monkeys. Journal of Neuroscience 7, 22852292.Google ScholarPubMed
Gaffan, D. & Murray, E.A. (1990). Amygdalar interaction with the mediodorsal nucleus of the thalamus and the ventromedial prefrontal cortex in stimulus-reward associative learning in the monkey. Journal of Neuroscience 10, 34793493.CrossRefGoogle ScholarPubMed
Gaffan, E.A., Gaffan, D. & Harrison, S. (1988). Disconnection of the amygdala from visual association cortex impairs visual reward-association learning in monkeys. Journal of Neuroscience 8, 31443150.CrossRefGoogle ScholarPubMed
Gallyas, F. (1979). Silver staining of myelin by means of physical development. Neurological Research 1, 203209.CrossRefGoogle ScholarPubMed
Gibson, A.R., Hansma, D.I., Houk, J.C. & Robinson, F.R. (1984). A sensitive low artifact TMB procedure for the demonstration of WGA-HRP in the CNS. Brain Research 298, 235241.CrossRefGoogle ScholarPubMed
Glickstein, M., Cohen, J.L., Dixon, B., Gibson, A., Hollins, M., Labossiere, E. & Robinson, F. (1980). Corticopontine visual projections in macaque monkeys. Journal of Comparative Neurology 190, 209229.CrossRefGoogle ScholarPubMed
Glickstein, M., May, J.G. III, & Mercier, B.E. (1985). Corticopontine projection in the macaque: The distribution of labelled cortical cells after large injections of horseradish peroxidase in the pontine nuclei. Journal of Comparative Neurology 235, 343359.CrossRefGoogle ScholarPubMed
Graham, J. (1982). Some topographical connections of the striate cortex with subcortical structures in Macaca fascicularis. Experimental Brain Research 47, 114.CrossRefGoogle ScholarPubMed
Graham, J., Lin, C.-S. & Kaas, J.H. (1979). Subcortical projections of six visual cortical areas in the owl monkey, Aotus trivirgatus. Journal of Comparative Neurology 187, 557580.CrossRefGoogle ScholarPubMed
Gross, C.G., Rocha-Miranda, C.E. & Bender, D.B. (1972). Visual properties of neurons in inferotemporal cortex of the macaque. Journal of Neurophysiology 35, 96111.CrossRefGoogle ScholarPubMed
Harting, J.K., Huerta, M.F., Frankfurter, A.J., Strominger, N.L. & Royle, G.J. (1980). Ascending pathways from the monkey superior colliculus: An autoradiographic analysis. Journal of Comparative Neurology 192, 853882.CrossRefGoogle ScholarPubMed
Iwai, E. & Yukie, M. (1987). Amygdalofugal and amygdalopetal connections with modality-specific visual cortical areas in macaques (Macaca fuscata, M. mulatta, and M. fascicularis). Journal of Comparative Neurology 261, 362387.CrossRefGoogle ScholarPubMed
Jones, E.G. & Burton, H. (1976). Areal differences in the laminar distribution of thalamic afferents in cortical fields of the insular, parietal and temporal regions of primates. Journal of Comparative Neurology 168, 197248.CrossRefGoogle ScholarPubMed
Jones, E.G., Wise, S.P. & Coulter, J.D. (1979). Differential thalamic relationships of sensory-motor and parietal cortical fields in monkeys. Journal of Comparative Neurology 183, 833882.CrossRefGoogle ScholarPubMed
Kemp, J.M. & Powell, T.P.S. (1970). The cortico-striate projection in the monkey. Brain 93, 525546.CrossRefGoogle ScholarPubMed
LeVay, S. & Sherk, H. (1981 a). The visual claustrum of the cat. I. Structure and connections. Journal of Neuroscience 9, 956980.CrossRefGoogle Scholar
LeVay, S. & Sherk, H. (1981 b). The visual claustrum of the cat. II. The visual field map. Journal of Neuroscience 9, 981992.CrossRefGoogle Scholar
Lock, T.M., Baizer, J.S. & Bender, D.B. (1990). Distribution of corticotectal cells in the superior temporal sulcus of the macaque. Society for Neuroscience Abstracts 14, 11.Google Scholar
Lynch, J.C., Graybiel, A.M. & Lobeck, L.J. (1985). The differential projection of two cytoarchitectonic subregions of the inferior parietal lobule of macaque upon the deep layers of the superior colliculus. Journal of Comparative Neurology 235, 241254.CrossRefGoogle ScholarPubMed
Mauguière, F. & Baleydier, C. (1978). Topographical organization of medial pulvinar neurons sending fibers to Brodmann’s areas 7, 21 and 22 in the monkey. Experimental Brain Research 31, 605607.CrossRefGoogle Scholar
Maunsell, J.H.R. & Newsome, W.T. (1987). Visual processing in monkey extrastriate cortex. Annual Review of Neuroscience 10, 363401.CrossRefGoogle ScholarPubMed
Maunsell, J.H.R. & Van Essen, D.C. (1983). The connections of the middle temporal visual area (MT) and their relationship to a cortical hierarchy in the macaque monkey. Journal of Neuroscience 3, 25632586.CrossRefGoogle ScholarPubMed
May, J.G. & Andersen, R.A. (1986). Different patterns of corticopontine projections from separate cortical fields within the inferior parietal lobule and prelunate gyrus of the macaque. Experimental Brain Research 63, 265268.CrossRefGoogle ScholarPubMed
Mesulam, M.-M. & Mufson, E.J. (1984). Neural inputs to the nucleus basalis of the substantia innominata (Ch4) in the rhesus monkey. Brain 107, 253274.CrossRefGoogle Scholar
Mesulam, M.-M., Mufson, E.J., Levey, A.I. & Wainer, B.H. (1983). Cholinergic innervation of cortex by the basal forebrain: Cytochemistry and cortical connections of the septal area, diagonal band nuclei, nucleus basalis (substantia innominata), and hypothalamus in the rhesus monkey. Journal of Comparative Neurology 214, 170190.CrossRefGoogle ScholarPubMed
Mesulam, M-M. & Van Hoesen, G.W., Pandya, D.N. & Geschwind, N. (1977). 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. Brain Research 136, 393414.CrossRefGoogle ScholarPubMed
Minciacchi, D., Granato, A. & Barbaresi, P. (1991). Organization of claustro-cortical projections to the primary somatosensory area of primates. Brain Research 553, 309312.CrossRefGoogle Scholar
Mishkin, M. (1982). A memory system in the monkey. Philosophical Transactions of the Royal Society B (London) 298, 8595.Google ScholarPubMed
Mizuno, N., Uchida, K., Nomura, S., Nakamura, Y., Sugimoto, T. & Uemura-Sumi, M. (1981). Extrageniculate projections to the visual cortex in the macaque monkey: an HRP study. Brain Research 212, 454459.CrossRefGoogle Scholar
Morel, A. & Bullier, J. (1990). Anatomical segregation of two cortical visual pathways in the macaque monkey. Visual Neuroscience 4, 555578.CrossRefGoogle ScholarPubMed
Murray, E.A. & Mishkin, M. (1984). Severe tactual as well as visual memory deficits follow combined removal of the amygdala and hippocampus in monkeys. Journal of Neuroscience 4, 25652580.CrossRefGoogle ScholarPubMed
Norden, J.J., Lin, C.-S. & Kaas, J.H. (1978). Subcortical projections of the dorsomedial visual area (DM) of visual association cortex in the owl monkey, Aotus trivirgatus. Experimental Brain Research 32, 321334.CrossRefGoogle ScholarPubMed
Olson, C.R. & Graybiel, A.M. (1980). Sensory maps in the claustrum of the cat. Nature 288, 479481.CrossRefGoogle ScholarPubMed
Olszewski, J. (1952). The Thalamus of Macaca Mulatta. Basel: S. Karger.Google Scholar
Partlow, G.D., Colonnier, M. & Szabo, J. (1977). Thalamic projections of the superior colliculus in the rhesus monkey, Macaca mulatta. A light and electron microscopic study. Journal of Comparative Neurology 171, 285318.CrossRefGoogle Scholar
Pearson, R.C.A., Brodal, P., Gatter, K.C. & Powell, T.P.S. (1982). The organization of the connections between the cortex and the claustrum in the monkey. Brain Research 234, 435441.CrossRefGoogle ScholarPubMed
Pearson, R.C.A., Brodal, P. & Powell, T.P.S. (1978). The projection of the thalamus upon the parietal lobe in the monkey. Brain Research 144, 143148.CrossRefGoogle ScholarPubMed
Petersen, S.E., Robinson, D.L. & Keys, W. (1985). Pulvinar nuclei of the behaving rhesus monkey: visual responses and their modulation. Journal of Neurophysiology 54, 867886.CrossRefGoogle ScholarPubMed
Pons, T.P. & Kaas, J.H. (1985). Connections of area 2 of somatosensory cortex with the anterior pulvinar and subdivisions of the ventroposterior complex in macaque monkeys. Journal of Comparative Neurology 240, 1636.CrossRefGoogle ScholarPubMed
Riche, D. & Lanoir, J. (1978). Some claustro-cortical connections in the cat and baboon as studied by retrograde horseradish peroxidase transport. Journal of Comparative Neurology 177, 435444.CrossRefGoogle Scholar
Robinson, D.L. & McClurkin, J.W. (1989). The visual superior colliculus and the pulvinar. In The Neurobiology of Saccadic Eye Movements, ed. Wurtz, R.H. & Goldberg, M.E., pp. 337360. Amsterdam: ElsevierGoogle Scholar
Robinson, D.L., Petersen, S.E. & Keys, W. (1986). Saccade-related and visual activities in the pulvinar nuclei of the behaving rhesus monkey. Experimental Brain Research 62, 625634.CrossRefGoogle ScholarPubMed
Saint-Cyr, J.A., Ungerleider, L.G. & Desimone, R. (1990). Organization of visual cortical inputs to the striatum and subsequent outputs to the pallido-nigral complex in the monkey. Journal of Comparative Neurology 298, 129156.CrossRefGoogle Scholar
Saunders, R.C., Murray, E.A. & Mishkin, M. (1984). Further evidence that amygdala and hippocampus contribute equally to visual recognition. Neuropsychologia 22, 785796.CrossRefGoogle Scholar
Schmahmann, J.D. & Pandya, D.N. (1989). Anatomical investigation of projections to the basis pontis from posterior parietal association cortex in rhesus monkey. Journal of Comparative Neurology 289, 5373.CrossRefGoogle Scholar
Schmahmann, J.D. & Pandya, D.N. (1990). Anatomical investigation of projections from thalamus to posterior parietal cortex in the rhesus monkey: a WGA-HRP and fluorescent tracer study. Journal of Comparative Neurology 295, 299326.CrossRefGoogle ScholarPubMed
Selemon, L.D. & Goldman-Rakic, P.S. (1985). Longitudinal topography and interdigitation of corticostriatal projections in the rhesus monkey. Journal of Neuroscience 5, 776794.CrossRefGoogle ScholarPubMed
Selemon, L.D. & Goldman-Rakic, P.S. (1988). 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. Journal of Neuroscience 8, 40494068.CrossRefGoogle ScholarPubMed
Sherk, H. (1986). The claustrum and the cerebral cortex. In Cerebral Cortex, Vol. 5, ed. Jones, E.G. & Peters, A. pp. 467499. New York: Plenum Press.Google Scholar
Spatz, W.B. (1975). Thalamic and other subcortical projections to area MT (visual area of the superior temporal sulcus) in the marmoset Callithrix jacchus. Brain Research 99, 129134.CrossRefGoogle ScholarPubMed
Spatz, W.B. & Tigges, J. (1973). Studies on visual area MT in primates. II. Projection fibers to subcortical structures. Brain Research 61, 374378.CrossRefGoogle ScholarPubMed
Spiegler, B. & Mishkin, M. (1981). Evidence for the sequential participation of inferior temporal cortex and amygdala in the acquisition of stimulus-reward associations. Behavioural Brain Research 3, 303317.CrossRefGoogle ScholarPubMed
Standage, G.P. & Benevento, L.A. (1983). The organization of connections between the pulvinar and visual area MT in the macaque monkey. Brain Research 262, 288294.CrossRefGoogle ScholarPubMed
Tigges, J., Tigges, M., Cross, N.A., McBride, R.L., Letbetter, W.D. & Anschel, S. (1982). Subcortical structures projecting to visual cortical areas in squirrel monkey. Journal of Comparative Neurology 209, 2940.CrossRefGoogle ScholarPubMed
Trojanowski, J.Q. & Jacobson, S. (1976). Areal and laminar distribution of some pulvinar cortical efferents in rhesus monkey. Journal of Comparative Neurology 169, 371392.CrossRefGoogle ScholarPubMed
Turner, B.H., Mishkin, M. & Knapp, M. (1980). Organization of the amygdalopetal projections from modality-specific cortical association areas in the monkey. Journal of Comparative Neurology 191, 515543.CrossRefGoogle ScholarPubMed
Ungerleider, L.G. & Desimone, R. (1986). Cortical connections of visual area MT in the macaque. Journal of Comparative Neurology 248, 190222.CrossRefGoogle ScholarPubMed
Ungerleider, L.G., Desimone, R., Galkin, T.W. & Mishkin, M. (1984). Subcortical projections of area MT in the macaque. Journal of Comparative Neurology 223, 368386.CrossRefGoogle ScholarPubMed
Ungerleider, L.G., Gaikin, T.W. & Mishkin, M. (1983). Visuotopic organization of projections from striate cortex to inferior and lateral pulvinar in rhesus monkey. Journal of Comparative Neurology 217, 135157.Google ScholarPubMed
Ungerleider, L.G. & Mishkin, M. (1982). Two cortical visual systems. In Analysis of Visual Behavior, ed. Ingle, D.J., Goodale, M.A. & Mansfield, R.J.W., pp. 549586. Cambridge, Massachusetts: MIT Press.Google Scholar
Van Hoesen, G.W., Yeterian, E.H. & Lavizzo-Mourey, R. (1981). Widespread corticostriate projections from temporal cortex of the rhesus monkey. Journal of Comparative Neurology 199, 205219.CrossRefGoogle ScholarPubMed
Weber, J.T. & Yin, T.C.T. (1984). Subcortical projections of the inferior parietal cortex (area 7) in the stump-tailed monkey. Journal of Comparative Neurology 224, 206230.CrossRefGoogle ScholarPubMed
Webster, M.J., Ungerleider, L.G. & Bachevalier, J. (1991 a). Subcortical connections of inferior temporal areas TE and TEO in macques. Society for Neuroscience Abstracts 17, 845.Google Scholar
Webster, M.J., Ungerleider, L.G. & Bachevalier, J. (1991 b). Connections of inferior temporal areas TE and TEO with medial temporal-lobe structures in infant and adult monkeys. Journal of Neuroscience 11, 10951116.CrossRefGoogle ScholarPubMed
Whitlock, D.G. & Nauta, W.J.H. (1956). Subcortical projections from the temporal neocortex in Macaca mulatta. Journal of Comparative Neurology 106, 183212.CrossRefGoogle Scholar
Yeterian, E.H. & Pandya, D.N. (1985). Corticothalamic connections of the posterior parietal cortex in the rhesus monkey. Journal of Comparative Neurology 237, 408426.CrossRefGoogle ScholarPubMed
Yeterian, E.H. & Van Hoesen, G.W. (1978). Cortico-striate projections in the rhesus monkey: The organization of certain cortico-cau-date connections. Brain Research 139, 4363.CrossRefGoogle ScholarPubMed