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Anatomical segregation of two cortical visual pathways in the macaque monkey

Published online by Cambridge University Press:  02 June 2009

Anne Morel  and
Jean Bullier
Anne Morel
Affiliation:
Vision et motricité. INSERM 94, 16 avenue du doyen Lépine 69500 Bron, France*
Jean Bullier
Affiliation:
Vision et motricité. INSERM 94, 16 avenue du doyen Lépine 69500 Bron, France*
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Abstract

A number of lines of evidence suggest that, in the macaque monkey, inferior parietal and inferotemporal cortices process different types of visual information. It has been suggested that visual information reaching these two subdivisions follows separate pathways from the striate cortex through the prestriate cortex. We examined directly this possibility by placing injections of the retrograde fluorescent tracers, fast blue and diamidino yellow, in inferior parietal and inferotemporal cortex and examining the spatial pattern of cortical areas containing labeled cells in two-dimensional reconstructions of the cortex.

The results of injections in inferotemporal cortex show that TEO receives afferents from areas V2, ventral V3, V3A, central V4, V4t, and DPL in prestriate cortex and from areas IPa, PGa, and FST in the superior temporal sulcus (STS). Area TEp receives afferents only from V4 in prestriate cortex and from IPa, PGa, and FST in the anterior STS. Area TEa receives no prestriate input and is innervated by IPa, PGa, FST, and TPO in the anterior STS.

The results of injections in inferior parietal cortex demonstrate that POa receives afferents from dorsal V3, V3A, peripheral V4, DPL, and PO in prestriate cortex, from MST and *VIP and from IPa, PGa, TPO, and FST in anterior STS. Area PGc (corresponding to 7a) is innervated by PO, MST, and by TPO in the anterior STS.

Examination of the two-dimensional reconstructions of the pattern of labeling after combined injections of fast blue and diamidino yellow in areas POa and TEO revealed that these areas are principally innervated by different prestriate areas. Only a small region, centered on area V3A and extending into V4 and DPL, contained cells labeled by either injection as well as a small number of double-labeled cells. In contrast, areas POa and TEO receive afferents from extensive common regions in the anterior STS corresponding to areas IPa, PGa, and FST.

These results directly demonstrate that visual information from the striate cortex reaches inferior parietal and inferotemporal cortices through largely separate prestriate cortical pathways. On the other hand, both parietal and inferotemporal cortices receive common inputs from extensive regions in the anterior STS which may play a role in linking the processing occurring in these two cortical subdivisions of the visual system.

Keywords

Prestriate cortexInferéotemporalInferior parietalDouble-labeling
Type
Research Articles
Information
Visual Neuroscience , Volume 4 , Issue 6 , June 1990 , pp. 555 - 578
Copyright
Copyright © Cambridge University Press 1990

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References

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.CrossRefGoogle ScholarPubMed
Balaudier, C. & Mauguier, 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.Google Scholar
Balzer, J.S., Ungerleider, L.G. & Desimone, R. (1988). Organization of visual projections to parietal and temporal cortex in the macaque. Society for Neuroscience Abstracts 8, 10.Google Scholar
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
Baylis, G.C., Rolls, E.T. & Leonard, C.M. (1987). Functional subdivisions of the temporal lobe neocortex. Journal Neuroscience 7, 330–342.CrossRefGoogle ScholarPubMed
Benevento, L.A., Fallon, J., Davis, B.J. & Rezak, M. (1977). Auditory-visual interaction in single cells in the cortex of the superior temporal sulcus and the orbital frontal cortex of the macaque monkey. Experimental Neurology 57, 849–872.CrossRefGoogle ScholarPubMed
Boussaoud, D., Ungerleider, L.G. & Desimone, R. (1988). Visual topography of area TEO in macaques. Neuroscience Abstract 85, 16.Google Scholar
Brodmann, K. (1909). Vergleichende Lokalisationslehre der Grosshirnrinde. Barth, J.A., Leipzig.Google Scholar
Bullier, J. (1990). Cortical visual areas in the macaque monkey. In Models of Visual Perception: From Natural to Artificial, ed. Imbert, M.Oxford University Press (in press).Google Scholar
Burkhalter, A. & Van Essen, D.C. (1986). Processing of color, form, and disparity information in visual areas VP and V2 of ventral extrastriate cortex in the macaque monkey. Journal of Neuroscience 6, 2327–2351.CrossRefGoogle ScholarPubMed
Cavada, C. & Goldman-Rakic, P.S. (1989 a). Posterior parietal cortex in rhesus monkey, I: Parcellation of areas based on distinctive limbic and sensory corticocortical connections. Journal of Comparative Neurology 287, 393–421.CrossRefGoogle ScholarPubMed
Cavada, C. & Goldman-Rakic, P.S. (1989 b). Posterior parietal cortex in rhesus monkey, II: Evidence for segregated corticocortical networks linking sensory and limbic areas with the frontal lobe. Journal of Comparative Neurology 287, 422–445.CrossRefGoogle ScholarPubMed
Colby, C.L., Gattass, R., Olson, C.R. & Gross, C.G. (1988). Topographical organization of cortical afferents to extrastriate visual area PO in the macaque: dual tracer study. Journal of Comparative Neurology 269, 392–413.CrossRefGoogle ScholarPubMed
Cusick, C.G. & Kaas, J.H. (1988). Cortical connections of area 18 and dorsolateral visual cortex in squirrel monkeys. Visual Neuroscience 1,211–238.CrossRefGoogle ScholarPubMed
Dean, P. (1976). Effects of inferotemporal lesions on the behavior of monkeys. Psychological Bulletin 83, 41–71.CrossRefGoogle ScholarPubMed
Dean, P. (1982). Visual behavior in monkeys with inferotemporal lesions. In Analysis of visual behavior, ed. Ingle, D.J., Goodale, M.A. & Mansfield, R.J.W., pp. 587–628, Cambridge, Massachusetts, MIT Press.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
Desimone, R. & Gross, C.G. (1979). Visual areas in the temporal cortex of the macaque. Brain Research, 178, 363–380.CrossRefGoogle ScholarPubMed
Desimone, R. & Ungerleider, L.G. (1986). Multiple visual areas in the caudal superior temporal sulcus of the macaque. Journal of Comparative Neurology 248, 164–189.CrossRefGoogle ScholarPubMed
DeYoe, E.A. & Van Essen, D.C. (1985). Segregation of efferent connections and receptive-field properties in visual area V2 of the macaque. Nature 317, 58–61.CrossRefGoogle ScholarPubMed
DeYoe, E.A. & Van Essen, D.C. (1988). Concurrent processing streams in monkey visual cortex. Trends in Neuroscience 11, 219–226.CrossRefGoogle ScholarPubMed
Felleman, D.J., Burkhalter, A. & Van Essen, D.C. (1987). Visual area PIP: An extrastriate cortical area in the posterior intraparietal sulcus of the macaque monkey. Society for Neuroscience Abstracts 13, 626.Google Scholar
Felleman, D.J. & Van Essen, D.C. (1987). Receptive-field properties of neurons in area V3 of macaque monkey extrastriate cortex. Journal of Neurophysiology 57, 889–920.CrossRefGoogle ScholarPubMed
Gallyas, F. (1979). Silver staining of myelin by means of physical development. Neurological Research 1, 203–209.CrossRefGoogle ScholarPubMed
Gaska, J.P., Jacobson, L.D. & Pollen, D.A. (1987). Response suppression by extending sine-wave gratings within the receptive fields of neurons in visual cortical area V3A of the macaque monkey. Vision Research 27, 1687–1692.CrossRefGoogle ScholarPubMed
Gattass, R., Gross, C.G. & Sandell, J.H. (1981). Visual topography of V2 in the macaque. Journal of Comparative Neurology 201, 519–539.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.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, 235–241.CrossRefGoogle ScholarPubMed
Gross, C.G. (1972). Inferotemporal cortex and vision. In Progress in Physiological Psychology, Vol. 5, ed. Stellar, E. & Sprague, J.M. pp. 77–123. New York: Academic Press.Google Scholar
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, 96–111.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Iwai, E. & Yukie, M. (1987). Amygdalofugal and amygdalopetal connections with modality-specific visual cortical areas in macaques (Macaca fuscata, Macaca mulatta, and Macaca fascicularis). Journal of Comparative Neurology 261, 362–387.CrossRefGoogle ScholarPubMed
Jones, E.G. & Powell, T.P.S. (1970). An anatomical study of converging sensory pathways within the cerebral cortex of the monkey. Brain 93, 793–820.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Klüver, H. & Bucy, P.C. (1937). “Psychic blindness” and other symptoms following bilateral temporal lobectomy in rhesus monkeys. American Journal of Physiology 119, 352–353.Google Scholar
Klüver, H., & Bucy, P.C. (1938). An analysis of certain effects of bilateral temporal lobectomy in the rhesus monkey, with special reference to “psychic blindness”. Journal of Psychology 5, 33–54.CrossRefGoogle Scholar
Komatsu, H. & Wurtz, R.H. (1988). Relation of cortical areas MT and MST to pursuit eye movements, I: Localization and visual properties of neurons. Journal of Neurophysiology 60, 580–603.CrossRefGoogle ScholarPubMed
Kuypers, H.G., Szwarcbart, M.K., Mishkin, M. & Rosvold, H.E. (1965). Occipito-temporal cortico-cortical cònnections in the rhesus monkey. Experimental Neurology 11, 245–262.CrossRefGoogle Scholar
Latto, R. (1986). The role of inferior parietal cortex and the frontal eye-fields in visuospatial discriminations in the macaque monkey. Behavioral Brain Research 22, 41–52.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Martin, K.A.C. (1988). From enzymes to visual perception: a bridge too far? Trends in Neuroscience 11, 380–387.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, 2563–2586.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, 393–414.CrossRefGoogle ScholarPubMed
Mishkin, M. (1954). Visual discrimination performance following partial ablations of the temporal lobe, II: Ventral surface vs. hippocampus. Journal of Comparative Physiology and Psychology 47, 187–193.CrossRefGoogle ScholarPubMed
Mishkin, M. (1966). Visual mechanisms beyond the striate cortex. In Frontiers in Physiological Psychology, ed. Russell, R., pp. 93–119, New York: Academic Press.Google Scholar
Mishkin, M. (1972). Cortical visual areas and their interactions. In Brain and Human Behavior, ed. Karczman, A. G. & Eccles, J. C. pp. 187–208, Berlin: Springer-Verlag.CrossRefGoogle Scholar
Mishkin, M. (1982). A memory system in the monkey. Philosophical Transactions of the Royal Society B, 298, 85–95.Google ScholarPubMed
Mishkin, M., Ungerleider, L.G. & Macko, K.A. (1983). Object vision and spatial vision: two cortical pathways. Trends in Neuroscience 6, 414–417.CrossRefGoogle Scholar
Morel, A. & Bullier, J. (1987). Cortical connections of intraparietal and inferotemporal visual areas in the macaque monkey: a double- labeling study. Society for Neuroscience Abstracts 177, 14.Google Scholar
Mountcastle, V.B., Lynch, J.C., Georgopoulos, A., Sakata, A. & Acuna, C. (1975). Posterior parietal association cortex of the monkey. Command functions for operations within extrapersonal space. Journal of Neurophysiology 38, 871–908.CrossRefGoogle ScholarPubMed
Neal, J.W., Pearson, R.C. A. & Powell, T.P.S. (1988 a). The corticocortical connections within the parieto-temporal lobe of area PG. 7a in the monkey. Brain Research 438, 343–350.CrossRefGoogle ScholarPubMed
Neal, J.W., Pearson, R.C.A. & Powell, T.P.S. (1988 b). The organization of the cortico-cortical connections between the walls of the lower part of the superior temporal sulcus and the inferior parietal lobule in the monkey. Brain Research 438, 351–356.CrossRefGoogle Scholar
Newsome, W.T., Maunsell, J.H.R. & Van Essen, D.C. (1986). Ventral posterior visual area of the macaque: visual topography and areal boundaries. Journal of Comparative Neurology 252, 139–153.CrossRefGoogle ScholarPubMed
Pandya, D.N. & Kuypers, H.G.J.M. (1969). Cortico-cortical connections in the rhesus monkey. Brain Research, 13, 13–36.CrossRefGoogle ScholarPubMed
Pandya, D.N. & Seltzer, B. (1982). Intrinsic connections and architectonics of posterior parietal cortex in the rhesus monkey. Journal of Comparative Neurology 204, 196–210.CrossRefGoogle ScholarPubMed
Perkel, D.H., Buller, J. & Kennedy, H. (1986). Topography of the afferent connectivity of area 17 of the macaque monkey: a double-labeling study. Journal of Comparative Neurology 253, 374–402.CrossRefGoogle Scholar
Petrides, M. & Iversen, S.D. (1979). Restricted posterior parietal lesions in the rhesus monkey and performance on visuospatial tasks. Brain Research 161, 63–77.CrossRefGoogle ScholarPubMed
Pohl, W. (1973). Dissociation of spatial discrimination deficits following frontal and parietal lesions in monkeys. Journal of Comparative Physiology and Psychology 82, 227–239.CrossRefGoogle ScholarPubMed
Sahgal, A. & Iversen, S.D. (1978). Categorization and retrieval after selective inferotemporal lesions in monkeys. Brain Research 146, 341–350.CrossRefGoogle ScholarPubMed
Saito, H., Yukie, M., Tanaka, K., Hikosaka, K., Fukada, Y. & Iwai, E. (1986). Integration of direction signals of image motion in the superior temporal sulcus of the macaque monkey. Journal of Neuroscience 6, 145–157.CrossRefGoogle ScholarPubMed
Schneider, G.E. (1969). Two visual systems. Science 163, 895–902.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, 1–24.CrossRefGoogle ScholarPubMed
Seltzer, B. & Pandya, D.N. (1980). Converging visual and somatic sensory cortical input to the intrapanietal sulcus of the rhesus monkey. Brain Research 192, 339–351.CrossRefGoogle Scholar
Seltzer, B. & Pandya, D.N. (1984). Further observations on parietotemporal connections in the monkey. Experimental Brain Research 55, 301–312.CrossRefGoogle ScholarPubMed
Seltzer, B. & Pandya, D.N. (1986). Posterior parietal projections to the intraparietal sulcus of the rhesus monkey. Experimental Brain Research 62, 459–469.CrossRefGoogle Scholar
Shibutami, H., Sakata, H. & Hyvarinen, J. (1984). Saccade and blinking evoked by microstimulation of the posterior parietal association cortex of the monkey. Experimental Brain Research 55, 1–8.Google Scholar
Shipp, S. & Zeki, S. (1985). Segregation of pathways leading from area V2 to areas V4 and V5 of macaque monkey visual cortex. Nature 315, 322–325.CrossRefGoogle ScholarPubMed
Shipp, S. & Zeki, S. (1989). The organization of connections between areas VS and V2 in macaque monkey visual cortex. European Journal of Neuroscience 1, 334–354.Google Scholar
Shiwa, T. (1987). Cortico-cortical projections to the monkey temporal lobe with particular reference to the visual processing pathways. Archives Italiennes de Biologie 125, 139–154.Google Scholar
Snyder, M. & Diamond, I.T. (1968). The organization and function of the visual cortex in the tree shrew. Brain Behavior and Evolution 1, 244–288.CrossRefGoogle Scholar
Tanaka, K., Hikosaka, K., Saito, H., Yukie, M., Fukada, Y. & Iwai, E. (1986). Analysis of local and wide-field movements in the superior temporal visual areas of the macaque monkey. Journal of Neuroscience 6, 134–144.CrossRefGoogle ScholarPubMed
Teuber, H.L. (1955). Physiological psychology. Annual Review of Psychology 6, 264–296.CrossRefGoogle ScholarPubMed
Trevarthen, C. (1968). Two mechanisms of vision in primate. Psychologishe Forschung 31, 299–337.CrossRefGoogle Scholar
Ungerleider, L.G. & Brody, B.A. (1977). Extrapersonal spatial orientation: the role of posterior panietal, anterior frontal, and inferotemporal cortex. Experimental Neurology 56, 265–280.CrossRefGoogle ScholarPubMed
Ungerleider, L.G. & Desimone, R. (1986). Cortical connections of visual area MT in the macaque. Journal of Comparative Neurology 248, 190–222.CrossRefGoogle ScholarPubMed
Ungerleider, L.G. & Mishkin, M. (1982). Two cortical visual systems. In Analysis of Visual Behavior, eds. Ingle, D.J., Goodale, M.A. & Mansfield, R.J.W. pp. 549–586, Cambridge, Massachusetts: MIT Press.Google Scholar
Van Essen, D.C. (1985). Functional organization of primate visual cortex. In Cerebral Cortex, Vol. 3, ed. Peters, A. & Jones, E.G., pp. 259–329, New York: Plenum Publishing Corporation.Google Scholar
Van Essen, D.C. & Maunsell, J.H.R. (1980). Two-dimensional maps of the cerebral cortex. Journal of Comparative Neurology 191, 255–281.CrossRefGoogle ScholarPubMed
Van Essen, D. C., Newsome, W. T., Maunsell, J.H.R. & Bixby, J.L. (1986). The projections from striate cortex (VI) to areas V2 and V3 in the macaque monkey: asymmetries, areal boundaries, and patchy connections. Journal of Comparative Neurology 244, 451–480.CrossRefGoogle Scholar
Van Essen, D.C. & Zeki, S.M. (1978). The topographic organization of rhesus monkey prestriate cortex. Journal of Physiology 277, 193–226.CrossRefGoogle Scholar
Von Bonin, G. & Bailey, P. (1947). The Neocortex of Macaca Mulatta. Urbana, Illinois: University of Illinois Press.Google Scholar
Weller, R.E. & Kaas, J.H. (1983). Retinotopic patterns of connections of area 17 with visual areas VII and MT in macaque monkeys. Journal of Comparative Neurology 220, 253–279.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Zeki, S.M. (1977). Color coding in the superior temporal sulcus of rhesus monkey visual cortex. Proceedings of the Royal Society B 197, 195–223.Google ScholarPubMed
Zeki, S.M. (1978). The third visual complex of rhesus monkey prestriate cortex. Journal of Physiology 277, 245–272.CrossRefGoogle ScholarPubMed
Zeki, S.M. & Shipp, S. (1988). The functional logic of cortical connections. Nature 335, 311–317.CrossRefGoogle ScholarPubMed