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Segregated thalamocortical pathways to inferior parietal and inferotemporal cortex in macaque monkey

Published online by Cambridge University Press:  02 June 2009

Christine Baleydier  and
Anne Morel
Christine Baleydier
Affiliation:
Vision et Motricité, INSERM 94, Bron, France
Anne Morel
Affiliation:
Vision et Motricité, INSERM 94, Bron, France
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Abstract

Inferior parietal and inferotemporal cortex, which process different aspects of visual information through largely segregated pathways from the visual cortex, both receive thalamic afferents from the pulvinar complex. We examined the topography of pulvinar projections to these two cortical regions by placing multiple injections of different tracers (fluorescent dyes, horseradish peroxidase) in the inferotemporal and inferior parietal cortex of macaque monkeys.

The patterns of label observed after injections in inferotemporal gyrus indicate that area TEO and the ventral part of area V4 receive a major input from the ventral part of the lateral pulvinar (PuLv) while area TE has strong connections with the caudal pole of the medial pulvinar (PuM) and only minor connections with PuLv. In contrast, injections in the caudal inferior parietal cortex demonstrate that area PGc, on the lateral surface of the inferior parietal gyrus, and area POa, in the ventral bank of intraparietal sulcus, receive strong projections from PuM and the adjacent fringe of the dorsal part of the lateral pulvinar (PuLd).

Paired injections of two different tracers in the inferotemporal and inferior parietal cortex of the same hemisphere revealed a nearly complete segregation of the two populations of labeled neurons in the pulvinar, with only a small region of overlap in PuM, close to the PuM/PuLd border. These results demonstrate a clear separation of the thalamic afferents to the inferior parietal and inferotemporal cortex which parallels the separation of prestriate afferents to these two cortical territories (Morel & Bullier, 1990).

Keywords

PulvinarInferotemporal and inferior/parietal cortexDouble-labeled study
Type
Research Articles
Information
Visual Neuroscience , Volume 8 , Issue 5 , May 1992 , pp. 391 - 405
Copyright
Copyright © Cambridge University Press 1992

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References

Acuna, C., Gonzalez, F. & Dominguez, R. (1983). Sensorimotor unit activity related to intention in the pulvinar of behaving Cebus apella monkeys. Experimental Brain Research 52, 411–422.CrossRefGoogle ScholarPubMed
Andersen, R.A., Asanuma, C. & Cowan, W.M. (1985). Callosal and prefrontal associational projecting cell populations in area 7a of the macaque monkey: a study using retrogradely transported fluorescent dyes. Journal of Comparative Neurology 232, 443–455.Google Scholar
Andersen, R.A., Asanuma, C., Essick, G. & Siegel, R.M. (1990). Corticocortical connections of anatomically and physiologically defined subdivisions within the inferior parietal lobule. Journal of Comparative Neurology 296, 65–113.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, 357–381.Google Scholar
Baizer, J.S., Ungerleider, L.G. & Desimone, R. (1991). Organization of visual inputs to inferior temporal and posterior parietal cortex in Macaques. Journal of Neuroscience 11, 168–190.CrossRefGoogle ScholarPubMed
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, 501–507.CrossRefGoogle Scholar
Baleydier, C. & Mauguière, F. (1980). The duality of the cingulate gyrus in monkey. Neuroanatomical study and functional hypothesis. Brain 103, 525–554.CrossRefGoogle ScholarPubMed
Baleydier, C. & Mauguière, F. (1985). Anatomical evidence for medial pulvinar connections with the posterior cingulate cortex, the retrosplenial area, and the parahippocampal gyrus in monkeys. Journal of Comparative Neurology 232, 219–228.CrossRefGoogle ScholarPubMed
Baleydier, C. & Mauguière, F. (1987). Network organization of the connectivity between parietal area 7, posterior cingulate cortex and medial pulvinar nucleus: A double fluorescent tracer study in monkey. Experimental Brain Research 66, 385–393.CrossRefGoogle ScholarPubMed
Barbas, H. & Mesulam, M.M. (1981). Organization of afferent input to subdivisions of area 8 in the rhesus monkey. Journal of Comparative Neurology 200, 407–431.CrossRefGoogle ScholarPubMed
Bender, D.B. (1981). Retinotopic organization of macaque pulvinar. Journal of Neurophysiology 46, 672–693.Google Scholar
Benevento, L.A. & Davis, B. (1977). Topographical projections of the prestriate cortex to the pulvinar nuclei in the macaque monkey: an autoradiographic study. Experimental Brain Research 30, 405–424.Google 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, 1–24.CrossRefGoogle ScholarPubMed
Benevento, L.A. & Standage, G.P. (1983). The organization of projections of the retinorecipient and nonretinorecipient nuclei of the pretectal complex and layers of the superior colliculus to the lateral pulvinar and medial pulvinar in the macaque monkey. Journal of Comparative Neurology 217, 307–336.CrossRefGoogle Scholar
Bos, J. & Benevento, L.A. (1977). Projections of the medial pulvinar to orbital cortex and frontal eye fields in the rhesus monkey (Macaca mulatta). Experimental Neurology 49, 487–496.CrossRefGoogle Scholar
Boussaoud, D., Ungerleider, L.G. & Desimone, R. (1990). Pathways for motion analysis: cortical connections of the medial superior temporal and fundus of the superior temporal visual areas in the macaque. Journal of Comparative Neurology 296, 462–495.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.Google Scholar
Burton, H. & Jones, E.G. (1976). The posterior thalamic region and its cortical projection in New World and Old World monkeys. Journal of Comparative Neurology 168, 249–302.Google Scholar
Cavada, C. & Goldman-Rakic, P.S. (1989). Posterior parietal cortex in rhesus monkey. 1. Parcellation of areas based on distinctive limbic and sensory corticocortical connections. Journal of Comparative Neurology 287, 393–421.CrossRefGoogle Scholar
Chow, K.L. (1950). A retrograde cell degeneration study of the cortical projection field of the pulvinar in the monkey. Journal of Comparative Neurology 93, 313–340.Google Scholar
Crouch, R.L. (1934). The nuclear configuration of the thalamus of Macacus rhesus. Journal of Comparative Neurology 59, 451–485.CrossRefGoogle Scholar
Desimone, R. & Gross, C.G. (1979). Visual areas in the temporal cortex of the macaque. Brain Research 178, 363–380.Google Scholar
Desimone, R., Flemming, J. & Gross, C.G. (1980). Prestriate afferents to inferior temporal cortex: an HRP study. Brain Research 184, 41–55.CrossRefGoogle ScholarPubMed
DeYoe, E.A. & Van Essen, D.C. (1988). Concurrent processing streams in monkey visual cortex. TINS 5, 219–226.Google Scholar
Divac, I., LaVail, J.H., Rakic, P. & Winston, K.R. (1977). Heterogeneous afferents to the inferior parietal lobule of the rhesus monkey revealed by retrograde transport method. Brain Research 123, 197–207.CrossRefGoogle Scholar
Fenstemaker, S.B., Sauceda, A.M., Albright, T.D. & Gross, C.G. (1986). A comparison of subcortical afferents to visual cortical areas V4, TEO and IT in the macaque. Society for Neuroscience Abstracts 12, 1364.Google Scholar
Friedmann, M. (1912). Die Cytoarchitektonik des Zwischenhirns der Cercopitheken mit besonderer Berücksichtigung des thalamus opticus. Journal für Psychologie und Neurologie 18, 309–378.Google Scholar
Gallyas, F. (1979). Silver staining of myelin by means of physical development. Neurology Research 1, 203–209.CrossRefGoogle ScholarPubMed
Gattass, R., Sousa, A.P.B. & Oswaldo-Cruz, E. (1978). Single unit response types in the pulvinar of the cebus monkey to multisensory stimulation. Brain Research 158, 75–87.CrossRefGoogle ScholarPubMed
Gattass, R., Sousa, A.P.B. & Gross, C.G. (1988). Visuotopic organization of V3 and V4 of the macaque. Journal of Neuroscience 8, 1831–1845.Google Scholar
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, 235–241.Google Scholar
Hardy, H., Heimer, L., Switzer, R. & Watkins, D. (1976). Simultaneous demonstration of horseradish peroxidase and acetylcholinesterase. Neuroscience Letters 3, 1–5.CrossRefGoogle ScholarPubMed
Iwai, E. & Mishkin, M. (1969). Further evidence on the locus of the visual area in the temporal lobe of the monkey. Experimental Neurology 25, 585–594.Google Scholar
Iwai, E. & Yukie, M. (1987). Amygdalofugal and amygdalopetal connections with modality-specific visual cortical areas in macaque (Macaca fuscata, Macaca mulatta and Macaca fascicularis). Journal of Comparative Neurology 261, 362–387.Google Scholar
Kaas, J.H. & Huerta, M.F. (1988). The subcortical visual system of primates. In Comparative Primate Biology Vol. 4: Neurosciences, ed. Setklis, H.D. & Erwin, J., pp. 327–391. New York: Liss.Google Scholar
Kasdon, D.L. & Jacobson, S. (1978). The thalamic afferents to the inferior parietal lobule of the rhesus monkey. Journal of Comparative Neurology 177, 685–706.Google Scholar
Kennedy, H. & Bullier, J. (1985). A double-labeling investigation of the afferent connectivity to cortical areas V1 and V2 of the macaque monkey. Journal of Neuroscience 5, 2815–2830.Google Scholar
Kievit, J. & Kuypers, H.G.J.M. (1977). Organization of the thalamo-cortical connexions to the frontal lobe in the rhesus monkey. Experimental Brain Research 29, 299–322.Google Scholar
Kikuchi, R. & Iwai, E. (1980). The locus of the posterior subdivision of the inferotemporal visual learning area in the monkey. Brain Research 198, 347–360.Google Scholar
Locke, S. (1960). The projection of the medical pulvinar of the Macaque. Journal of Comparative Neurology 115, 155–167.CrossRefGoogle 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, 241–254.Google Scholar
Lysakowski, A., Standage, G.P. & Benevento, L.A. (1988). An investigation of collateral projections of the dorsal lateral geniculate nucleus and other subcortical structures to cortical areas VI and V4 in the macaque monkey: a double label retrograde study. Experimental Brain Research 69, 651–661.Google Scholar
Magarinos-Ascone, C., BuniW., Jr. W., Jr. & Garcia-Austt, E. (1988). Monkey pulvinar units related to motor activity and sensory response. Brain Research 445, 30–38.Google Scholar
Markowitsch, H.J., Emmans, D., Irle, E., Streicher, M., & Prelowski, B. (1985). Cortical and subcortical afferent connections of the primate's temporal pole: a study of rhesus monkeys, squirrel monkeys and marmosets. Journal of Comparative Neurology 242, 425–458.CrossRefGoogle Scholar
Mathers, L.H. & Rapisardi, S.C. (1973). Visual and somatosensory receptive fields of neurons in the pulvinar of the squirrel monkey. Brain Research 64, 65–84.Google Scholar
May, J.G. & Andersen, R.A. (1986). Different patterns of corticopontine projections from separate cortical fields within the inferior parietal lobule and dorsal prelunate gyrus of the macaque. Experimental Brain Research 63, 265–278.CrossRefGoogle ScholarPubMed
Mesulam, M.M. (1981). A cortical network for directed attention and unilateral neglect. Annual Review of Neurology 10, 309–325.Google Scholar
Mesulam, M.M. (1990). Large-scale neurocognitive networks and distributed processing for attention, language, and memory. Annual Review of Neurology 28, 597–613.Google Scholar
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, 393–414.CrossRefGoogle ScholarPubMed
Mishkin, M. (1982). A memory system in the monkey. Philosophical Transactions of the Royal Society B (London) 298, 85–95.Google Scholar
Mishkin, M., Ungerleider, L.G. & Macko, K.A. (1983). Object vision and spatial vision: two cortical pathways. Trends in Neuroscience 6, 414–417.Google Scholar
Moran, M.A., Mufson, E.J. & Mesulam, M.M. (1987). Neural inputs into the temporopolar cortex of the rhesus monkey. Journal of Comparative Neurology 256, 88–103.Google Scholar
Morel, A. & Bullier, J. (1990). Anatomical segregation of two cortical visual pathways in the macaque monkey. Visual Neuroscience 4, 555–578.Google Scholar
Olszewski, J. (1952). The Thalamus of the Macaca mulatta. Basel: Karger.Google Scholar
Pandya, D.N. & Selzer, B. (1982). Intrinsic connections and architectonics of posterior parietal cortex in the rhesus monkey. Journal of Comparative Neurology 204, 196–210.Google 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, 435–441.Google Scholar
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, 143–148.CrossRefGoogle ScholarPubMed
Pohl, W. (1973). Dissociation of spatial discrimination deficits following frontal and parietal lesions. Journal of Comparative Physiology and Psychology 82, 227–239.Google 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, 299–326.Google Scholar
Selzer, 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, 1–24.Google Scholar
Selzer, B., & Pandya, D.N. (1980). Converging visual and somatic sensory cortical input to the intraparietal sulcus in the rhesus monkey. Brain Research 192, 339–351.Google Scholar
Siqueira, E.B. (1965). The temporo-pulvinar connections in the rhesus monkey. Archives of Neurology 13, 321–330.CrossRefGoogle ScholarPubMed
Stanton, G.B., Cruce, W.L.R., Goldberg, M.E. & Robinson, D.L. (1977). Some ipsilateral projections to areas PF and PG of the inferior parietal lobule in monkeys. Neuroscience Letters 6, 243–250.Google Scholar
Trojanowski, J.Q. & Jacobson, S. (1974). Medial pulvinar afferents to frontal eye-fields in rhesus monkey demonstrated by horseradish peroxidase. Brain Research 80, 395–411.Google Scholar
Trojanowski, J.Q. & Jacobson, S. (1976). Areal and laminar distribution of some pulvinar cortical efferents in rhesus monkey. Journal of Comparative Neurology 169, 371–392.Google Scholar
Ungerleider, L.C. & Christensen, C.A. (1977). Pulvinar lesions in monkeys produce abnormal eye movements during visual discrimination training. Brain Research 136, 189–196.Google Scholar
Ungerleider, L.G. & Christensen, C.A. (1979). Pulvinar lesions in monkeys produce abnormal scanning of a complex visual array. Neuropsychology 17, 493–501.Google Scholar
Ungerleider, L.G., Galkin, 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, 137–157.CrossRefGoogle 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. 549–586. Cambridge, MA: MIT Press.Google Scholar
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.Google Scholar
Von Bonin, G. & Bailey, P. (1947). The Neocortex of Macaca Mulatta. Urbana, IL: University of Illinois Press, 165p.Google Scholar
Walker, A.E. (1937). A note on the thalamic nuclei of Macaca mulatta. Journal of Comparative Neurology 66, 145–155.Google Scholar
Weber, J.T. & Yin, T.C.T. (1984). Subcortical projections of the inferior parietal cortex (area 7) in the stumptailed monkey. Journal of Comparative Neurology 224, 206–230.Google Scholar
Whitlock, D.G. & Nauta, W.J.H. (1956). Subcortical projections from the temporal neocortex in Macaca mulatta. Journal of Comparative Neurology 106, 183–212.Google Scholar
Wong-Riley, M. (1979). Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry. Brain Research 171, 11–28.Google Scholar
Yeterian, E.H. & Pandya, D.N. (1988). Cortico-thalamic connections of paralimbic regions in the rhesus monkey. Journal of Comparative Neurology 269, 130–146.Google Scholar
Yeterian, E.H. & Pandya, D.N. (1989). Thalamic connections of the cortex of the superior temporal sulcus in the rhesus monkey. Journal of Comparative Neurology 282, 80–97.Google Scholar
Yeterian, E.H. & Van Hoesen, G.W. (1978). Cortico-striate projections in the rhesus monkey: the organization of certain corticocaudate connections. Brain Research 139, 43–63.Google Scholar