Hostname: page-component-848d4c4894-m9kch Total loading time: 0 Render date: 2024-05-31T20:51:18.529Z Has data issue: false hasContentIssue false

Subcortical connections of visual areas MST and FST in macaques

Published online by Cambridge University Press:  02 June 2009

Driss Boussaoud
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
*
Address all correspondence and reprint requests to: Leslie G. Ungerleider, Laboratory of Neuropsychology, National Institute of Mental Health, Building 9, Room 1E104, Bethesda, MD 20892, USA.

Abstract

To examine the subcorctical connections of the medial superior temporal and fundus of the superior temporal visual areas (MST and FST, respectively), we injected anterograde and retrograde tracers into 16 physiologically identified sites within the two areas in seven macaque monkeys. The subcortical connections of MST and FST were found to be very similar. Both areas were found to be reciprocally connected with the pulvinar, mainly with its medial subdivision, and with the claustrum. Nonreciprocal projections from both MST and FST were consistently found in the striatum (caudate and putamen), reticular nucleus of the thalamus, and the pontine nuclei. The labeled terminals in the pons were in the dorsolateral, lateral, dorsal, and peduncular nuclei. Additional nonreciprocal projections were found in one MST and one FST case to the nucleus of the optic tract, and, in one FST case, to the lateral terminal nucleus. Finally, three cases showed a nonreciprocal projection to FST from the basal forebrain. The subcortical structures containing label following MST and FST injections were largely the same as those labeled after injections of the middle temporal visual area (MT), but the label within each structure after MST and FST injections was more widespread than that from MT, overlapping the distribution of label that has been reported after injections of parietal visual areas. This finding is consistent with the known contributions of MST and FST to the functions of parietal cortex, such as eye-movement control.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1992

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Albright, T.D., Desimone, R. & Gross, C.G. (1984). Columnar organization of directionally selective cells in visual area MT of the macaque. Journal of Neurophysiology 51, 1631.CrossRefGoogle ScholarPubMed
Allman, J.M. & Kaas, J.H. (1971). A representation of the visual field in the caudal third of the middle temporal gyrus of the owl monkey (Aotus trivirgatus). Brain Research 31, 85105.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). Subcortical connections of inferior temporal and posterior parietal cortex in macaques. Society for Neuroscience Abstracts 17, 845.Google Scholar
Baker, J.F., Petersen, S.E., Newsome, W.T. & Allman, J.M. (1981). Visual response properties of neurons in four extrastriate visual areas of the owl monkey (Aotus trivirgatus): A quantitative comparison of medial, dorsomedial, dorsolateral, and middle temporal areas. Journal of Neurophysiology 45, 397416.CrossRefGoogle ScholarPubMed
Bender, D.B. (1981). Retinotopic organization of macaque pulvinar. Journal of Neurophysiology 46, 672693.CrossRefGoogle ScholarPubMed
Boussaoud, D., Ungerleider, L.G. & Desimone, R. (1989). Subcortical connections of visual areas MST and FST in macaques. Society for Neuroscience Abstracts 15, 1399.Google 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, 462495.CrossRefGoogle ScholarPubMed
Brodal, P. (1978). The corticopontine projection in the rhesus monkey: Origin and principles of organization. Brain 101, 251283.CrossRefGoogle ScholarPubMed
Brodal, P. (1982). Further observations on the cerebellar projections from the pontine nuclei and the nucleus reticularis tegmenti pontis in the rhesus monkey. Journal of Comparative Neurology 204, 4455.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 temporal cortex of the macaque. Brain Research 178, 363380.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, 164189.CrossRefGoogle ScholarPubMed
Dürsteler, M.R. & Wurtz, R.H. (1988). Pursuit and optokinetic deficits following chemical lesions of cortical areas MT and MST. Journal of Neurophysiology 60, 940965.CrossRefGoogle ScholarPubMed
Dürsteler, M.R., Wurtz, R.H. & Newsome, W.T. (1987). Directional pursuit deficits following lesions of the foveal representation within the superior temporal sulcus of the macaque monkey. Journal of Neurophysiology 57, 12621287.CrossRefGoogle ScholarPubMed
Felleman, D.J. & Kaas, J.H. (1984). Receptive field properties of neurons in the middle temporal visual area (MT) of owl monkeys. Journal of Neurophysiology 52, 488513.CrossRefGoogle ScholarPubMed
Felleman, D.J. & Van Essen, D.C. (1991). Distributed hierarchical processing in the primate cerebral cortex. Cerebral Cortex 1, 147.CrossRefGoogle ScholarPubMed
Fiorani, M. Jr, Gattass, R., Rosa, M.G.P. & Sousa, A.P.B. (1989). Visual area MT in the Cebus monkey: Location, visuotopic organization, and variability. Journal of Comparative Neurology 287, 98118.CrossRefGoogle ScholarPubMed
Fries, W. (1990). Pontine projection from striate and prestriate visual cortex in the macaque monkey: An anterograde study. Visual Neuroscience 4, 205216.CrossRefGoogle ScholarPubMed
Galletti, C., Maioli, M.G., Squatrito, S. & Battagini, P.P. (1982). Corticopontine projections from the visual area of the superior temporal sulcus in the macaque monkey. Archives of Italian Biology 120, 411417.Google 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., 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
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
Hoffmann, K.-P. & Distler, C. (1989). Quantitative analysis of visual receptive fields of neurons in nucleus of the optic tract and dorsal terminal nucleus of the accessory optic tract in macaque monkey. Journal of Neurophysiology 62, 416428.CrossRefGoogle ScholarPubMed
Hoffmann, K.-P., Distler, C., Erickson, R.G. & Mader, W. (1988). Physiological and anatomical identification of the nucleus of the optic tract and dorsal terminal nucleus of the accessory optic tract in monkeys. Experimental Brain Research 69, 635644.CrossRefGoogle ScholarPubMed
Kase, M., Noda, H., Suzuki, D.A. & Miller, D.C. (1979). Target velocity signals of visual tracking in vermal Purkinje cells of the monkey. Science 205, 717720.CrossRefGoogle ScholarPubMed
Komatsu, H. & Wurtz, R.H. (1988a). Relation of cortical areas MT and MST to pursuit eye movements. I. Localization and visual properties of neurons. Journal of Neurophysiology 60, 580603.CrossRefGoogle ScholarPubMed
Komatsu, H. & Wurtz, R.H. (1988b). Relation of cortical areas MT and MST to pursuit eye movements. III. Interaction with full-field visual stimulation. Journal of Neurophysiology 60, 621644.CrossRefGoogle ScholarPubMed
Komatsu, H. & Wurtz, R.H. (1989). Modulation of pursuit eye movements by stimulation of cortical areas MT and MST. Journal of Neurophysiology 62, 3147.CrossRefGoogle ScholarPubMed
Langer, T.P., Fuchs, A.F., Scudder, C. & Chubb, M.C. (1985). Aferents to the flocculus of the cerebellum in the rhesus macaque as revealed by retrograde transport of horseradish peroxidase. Journal of Comparative Neurology 235, 125.CrossRefGoogle Scholar
Lisberger, S.G. & Fuchs, A.F. (1978). Role of primate flocculus during rapid behavioral modification of vestibulo-ocular reflex. I. Purkinje cell activity during visually guided horizontal smooth pursuit eye movement and passive head rotation. Journal of Neurophysiology 41, 733763.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 16, 110.Google Scholar
Maekawa, K. & Simpson, J.I. (1973). Climbing fiber responses evoked in vestibulocerebellum of rabbit from visual system. Journal of Neurophysiology 36, 649666.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 dorsal prelunate gyrus of the macaque. Experimental Brain Research 63, 265278.CrossRefGoogle ScholarPubMed
Mesulam, M.-M. (1978). Tetramethyl benzidine for horseradish peroxidase neurohistochemistry: A non-carcinogenic blue reactionproduct with superior sensitivity for visualizing neural afferents and efferents. Journal ofHistochemistry and Cytochemistry 26, 106117.CrossRefGoogle ScholarPubMed
MESULAM, M.-M., Mufson, E.J., & Wainer, B.H. (1986). Three-dimensional representation and cortical projection topography of the nucleus basalis (Ch4) in the macaque: Concurrent demonstration of choline acetyltransferase and retrograde transport with stabilized tetramethylbenzidine method for horseradish peroxidase. Brain Research 367, 301308.CrossRefGoogle ScholarPubMed
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
Mustari, M.J. & Fuchs, A.F. (1989). Response properties of single units in the lateral terminal nucleus of the accessory optic system in the behaving primate. Journal of Neurophysiology 61, 12071220.CrossRefGoogle ScholarPubMed
Mustari, M.J., Fuchs, A.F. & Wallman, J. (1988). Response properties of dorsolateral pontine units during smooth pursuit in the rhesus macaque. Journal of Neurophysiology 460, 664686.CrossRefGoogle Scholar
Newsome, W.T. & Pare, E.B. (1988). A selective impairment of motion perception following lesions of the middle temporal visual area (MT). Journal of Neuroscience 8, 22012211.CrossRefGoogle ScholarPubMed
Newsome, W.T., Wurtz, R.H. & Komatsu, H. (1988). Relation of cortical areas MT and MST to pursuit eye movements. II. Differentiation of retinal from extraretinal inputs. Journal of Neurophysiology 60, 604620.CrossRefGoogle ScholarPubMed
Newsome, W.T., Wurtz, R.H., Dürsteler, M.R. & Mikami, A. (1985). Deficits in visual motion processing following ibotenic acid lesions of the middle temporal visual area of the macaque monkey. Journal of Neuroscience 5, 825840.CrossRefGoogle ScholarPubMed
Noda, H. & Suzuki, D.A. (1979). The role of the flocculus of the monkey in fixation and smooth pursuit eye movements. Journal of Physiology (London) 294, 335348.CrossRefGoogle ScholarPubMed
Nyby, O. & Jansen, J. (1951). An experimental investigation of the corticopontine projection in Macaca mulatto. Skrifter utgitt av del Norske Videnskaps-Akademi 3, 147.Google Scholar
Rosene, D.L., Roy, N.J. & Davis, B.J. (1986). A cryoprotection method that facilitates cutting frozen sections of whole monkey brains from histological and histochemical processing without freezing artifact. Journal of Histochemistry and Cytochemistry 34, 13011315.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
Sekiya, H. & Kawamura, K. (1985). An HRP study in the monkey of olivary projections from the mesodiencephalic structures with particular reference to pretecto-olivary neurons. Archives of Italian Biology 123, 171183.Google ScholarPubMed
Siegel, R.M. & Andersen, R.A. (1986). Motion perceptual deficits following ibotenic acid lesions of the middle temporal area (MT) in the behaving rhesus monkey. Society for Neuroscience Abstracts 12, 1183.Google Scholar
Spatz, W.B. & Tioges, J. (1972). Experimental-anatomical studies on the “middle temporal visual area (MT)” in primates. I. Efferent cortico-cortical connections in the marmoset Callithrix jacchus. Journal of Comparative Neurology 146, 451464.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
Suzuki, D.A. & Keller, E.L. (1984). Visual signals in the dorsolateral pontine nucleus of the alert monkey: Their relationship to smoothpursuit eye movements. Experimental Brain Research 53, 473478.CrossRefGoogle ScholarPubMed
Suzuki, D.A., Noda, H. & Kase, M. (1981). Visual and pursuit eye movement-related activity in posterior vermis of monkey cerebellum. Journal of Neurophysiology 46, 11201139.CrossRefGoogle ScholarPubMed
Suzuki, D.A., May, J. & Keller, E.L. (1984). Smooth-pursuit eye movement deficits with pharmacological lesions in monkey dorsolateral pontine nucleus. Society for Neuroscience Abstracts 10, 58.Google Scholar
Suzuki, D.A., May, J.G., Keller, E.L. & Yee, R.D. (1990). Visual motion response properties of neurons in dorsolateral pontine nucleus of alert monkey. Journal of Neurophysiology 63, 3759.CrossRefGoogle ScholarPubMed
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, 134144.CrossRefGoogle ScholarPubMed
Tusa, R.J. & Ungerleider, L.G. (1988). Fiber pathways of cortical areas mediating smooth pursuit eye movements in monkeys. Annals of Neurology 23, 174183.CrossRefGoogle ScholarPubMed
Ungerleider, L.G. & Desimone, R. (1986). Cortical projections of visual area MT in the macaque. Journal of Comparative Neurology 248, 190222.CrossRefGoogle ScholarPubMed
Ungerleider, L.G. & Mishkin, M. (1979). The striate projection zone in the superior temporal sulcus of Macaca mulatto: Location and topographic organization. Journal of Comparative Neurology 188, 347366.CrossRefGoogle Scholar
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
Vandenbussche, E., Saunders, R.C. & Orban, G.A. (1991). Lesions of MT impair speed discrimination performance in the Japanese monkeys (Macaca fuscata). Society for Neuroscience Abstracts 17, 8.Google Scholar
Van Essen, D.C. & Maunsell, J.H.R. (1980). Two-dimensional maps of the cerebral cortex. Journal of Comparative Neurology 191, 255281.CrossRefGoogle ScholarPubMed
Van Essen, D.C., Maunsell, J.H.R. & Bixby, J.L. (1981). The middle temporal visual area in the macaque: Myeloarchitecture, connections, functional properties and topographic organization. Journal of Comparative Neurology 199, 293326.CrossRefGoogle ScholarPubMed
Webster, M.J., Ungerleider, L.G. & Bachevalier, J. (1991). Subcortical connections of inferior temporal areas TE and TEO in macaques. Society for Neuroscience Abstracts 17, 845.Google Scholar
Weller, R.E., Wall, J.T. & Kaas, J.H. (1984). Cortical connections of the middle temporal visual area (MT) and the superior temporal sulcus in owl monkeys. Journal of Comparative Neurology 228, 81104.CrossRefGoogle ScholarPubMed
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, 8097.CrossRefGoogle ScholarPubMed
Yeterian, E.H. & Pandya, D.N. (1991). Corticothalamic connections of the superior temporal sulcus in rhesus monkeys. Experimental Brain Research 83, 268284.CrossRefGoogle ScholarPubMed
Zeki, S.M. (1974). Functional organization of a visual area in the posterior bank of the superior temporal sulcus of the rhesus monkey. Journal of Physiology (London) 236, 549573.CrossRefGoogle ScholarPubMed
Zeki, S.M. (1978a). Uniformity and diversity of structure and function in rhesus monkey prestriate visual cortex. Journal of Physiology (London) 277, 273290.CrossRefGoogle ScholarPubMed
Zeki, S.M. (1978b). Functional specialization in the visual cortex of the rhesus monkey. Nature (London) 274, 423428.CrossRefGoogle ScholarPubMed