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Area 17 lesions deactivate area MT in owl monkeys

Published online by Cambridge University Press:  02 June 2009

Jon H. Kaas
Affiliation:
Department of Psychology, Vanderbill University, Nashville
Leah A. Krubitzer
Affiliation:
Department of Psychology, Vanderbill University, Nashville

Abstract

The middle temporal visual area, MT, is one of three major targets of the primary visual cortex, area 17, in primates. We assessed the contribution of area 17 connections to the responsiveness of area MT neurons to visual stimuli by first mapping the representation of the visual hemifield in MT of anesthetized owl monkeys with microelectrodes, ablating an electrophysiologically mapped part of area 17, and then immediately remapping MT. Before the lesions, neurons at recording sites throughout MT responded vigorously to moving slits of light and other visual stimuli. In addition, the relationship of receptive fields to recording sites revealed a systematic representation of the contralateral visual hemifield in MT, as reported previously for owl monkeys and other primates. The immediate effect of removing part of the retinotopic map in area 17 by gentle aspiration was to selectively deactivate the corresponding part of the visuotopic map in MT. Lesions of dorsomedial area 17 representing central and paracentral vision of the lower visual quadrant deactivated neurons in caudomedial MT formerly having receptive fields in the central and paracentral lower visual quadrant. Most neurons at recording sites throughout other parts of MT had normal levels of responsiveness to visual stimuli, and receptive-field locations that closely matched those before the lesion. However, neurons at a few sites along the margin of the deactivated zone of cortex had receptive fields that were slightly displaced from the region of vision affected by the lesion into other parts of the visual field, suggesting some degree of plasticity in the visual hemifield representation in MT. Subsequent histological examination of cortex confirmed that the lesions were confined to area 17 and the recordings were in MT. The results indicate that the visually evoked activity of neurons in MT of owl monkeys is highly dependent on inputs relayed directly or indirectly from area 17.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1992

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References

Albright, T.D. & Desimone, R. (1987). Local precision of visuotopic organization in the middle temporal area (MT) of the macaque. Experimental Brain Research 65, 582592.CrossRefGoogle ScholarPubMed
Allman, J.M. & Kaas, J.H. (1971a). A representation of the visual field in the posterior third of the middle temporal gyrus of the owl monkey (Aotus trivirgalus). Brain Research 31, 85105.CrossRefGoogle Scholar
Allman, J.M. & Kaas, J.H. (1971b). Representation of the visual field in striate and adjoining cortex of the owl monkey (Aotus trivirgatus). Brain Research 35, 89106.CrossRefGoogle ScholarPubMed
Allman, J.M. & Kaas, J.H. (1974). The organization of the second vi- sual area (VII) in the owl monkey: A second order transformation of the visual hemifield. Brain Research 76, 247265.CrossRefGoogle Scholar
Allman, J.M., Kaas, J.H. & Lane, R.H. (1973). The middle temporal visual area (MT) in the bush baby (Calago senegalensis). Brain Research 57, 197202.CrossRefGoogle Scholar
Bender, D.B. (1983). Visual activation of neurons in the primate pulvinar depends on cortex but not colliculus. Brain Research 279, 258261.CrossRefGoogle Scholar
Benevento, L.A. & Standage, G.P. (1982). Demonstration of lack of dorsal lateral geniculate input to extrastriate areas MT and visual area 2 in the macaque monkey. Monkey Brain Research 252, 161166.CrossRefGoogle Scholar
Benevento, L.A. & Yoshida, K. (1981). The afferent and efferent organization of the lateral geniculo-prestriate pathways in the macaque monkey. Journal of Comparative Neurology 203, 455474.CrossRefGoogle ScholarPubMed
Bruce, C., Desimone, R. & Gross, C.G. (1986). Both striate cortex and the superior colliculus contribute to the visual properties of neurons in the superior temporal polysensory area in the macaque. Journal of Neurophysiology 55, 10571075.CrossRefGoogle Scholar
Bullier, J. & Girard, P. (1988). Visual responses of neurons in area V2 and in the superior temporal sulcus of the macaque monkey during reversible inactivations of area V1. Society for Neuroscience Abstracts 14, 602.Google Scholar
Bullier, J. & Kennedy, H. (1983). Projection of the lateral geniculate nucleus onto cortical area V2 in the macaque monkey. Experimental Brain Research 53, 168172.CrossRefGoogle ScholarPubMed
Burman, D.G., Felsten, G. & Benevento, L.A. (1982). Visual properties of neurons in the lateral pulvinar of normal and occipital lobectomised macaques. Investigative Ophthalmology and Visual Science 22, 237.Google Scholar
Cowey, A. & Stoerig, P. (1989). Projection patterns of surviving neurons in the dorsal lateral geniculate nucleus following discrete lesions of striate cortex: Implications for residual vision. Experimental Brain Research 75, 631638.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, 5861.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
Fernald, R. & Chase, R. (1971). An improved method for plotting retinal landmarks and focusing the eyes. Vision Research 11, 9596.CrossRefGoogle ScholarPubMed
Fiorani, M., 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
Gallyas, F. (1979). Silver staining of myelin by means of physical development. Neurological Research 1, 203209.CrossRefGoogle ScholarPubMed
Gattass, R. & Gross, C.G. (1981). Visual topography of the striate projection zone in the posterior superior temporal sulcus (MT) of the macaque. Journal of Neurophysiology 46, 621638.CrossRefGoogle ScholarPubMed
Girard, P. & Bullier, J. (1989). Visual activity in area V2 during reversible inactivation of area 17 in the macaque monkey. Journal of Neurophysiology 62, 12871302.CrossRefGoogle ScholarPubMed
Girard, P., Salin, P.A. & Bullier, J. (1991). Visual activity in macaque area V4 depends on area 17 input. Neuroreporl 2, 8184.CrossRefGoogle ScholarPubMed
Harting, J.K., Huerta, M.F., Frankfurter, A.J., Strominger, N.L. & Royce, G.J. (1980). Ascending pathways from the monkey superior colliculus: an autoradiographic analysis. Journal of Comparative Neurology 192, 853882.CrossRefGoogle ScholarPubMed
Kaas, J.H. (1991). Plasticity of sensory and motor maps in adult mammals. Annual Review of Neuroscience 14, 137167.CrossRefGoogle ScholarPubMed
Kaas, J.H. & Huerta, M.F. (1988). Subcortical visual system of primates. In Comparative Primate Biology, Vol. 4: Neuroscience, ed. Steklis, H.P., pp. 327391. New York: Alan R. Liss, Inc.Google Scholar
Kaas, J.H., Huerta, M.F., Weber, J.T. & Harting, J.K. (1978). Patterns of retinal terminations and laminar organization of the lateral geniculate nucleus of primates. Journal of Comparative Neurology 182, 517554.CrossRefGoogle ScholarPubMed
Kaas, J.H., Krubitzer, L.A., Chino, Y.M., Langston, A.L., Polley, E.H. & Blair, N. (1990). Reorganization of retinotopic cortical maps in adult mammals after lesions of the retina. Science 248, 229231.CrossRefGoogle ScholarPubMed
Kaas, J.H., Lin, C.-S. & Casagrande, V.A. (1976). The relay of ipsilateral and contralateral retinal input from the lateral geniculate nucleus to striate cortex in the owl monkey: A transneuronal transport study. Brain Research 106, 371378.CrossRefGoogle ScholarPubMed
Krubitzer, L.A. & Kaas, J.H. (1989a). Cortical integration of parallel pathways in the visual system of primates. Brain Research 478, 161165.CrossRefGoogle ScholarPubMed
Krubitzer, L.A. & Kaas, J.H. (1989b). Striate cortex lesions in monkeys deactivate neurons in the middle temporal visual area (MT). Investigative Ophthalmology and Visual Science (Suppl.) 30, 299.Google Scholar
Krubitzer, L.A. & Kaas, J.H. (1990a). Cortical connections of MT in four species of primates: Areal, modular, and retinotopic patterns. Visual Neuroscience 5, 165204.CrossRefGoogle ScholarPubMed
Krubitzer, L.A. & Kaas, J.H. (1990b). Convergence of processing channels in extrastriate cortex of monkeys. Visual Neuroscience 5, 609613.CrossRefGoogle ScholarPubMed
LIN, C.-S. & Kaas, J.H. (1979). The inferior pulvinar complex in owl monkeys: Architectonic subdivisions and patterns of input from the superior colliculus and subdivisions of visual cortex. Journal of Comparative Neurology 187, 655678.CrossRefGoogle ScholarPubMed
LIN, C.-S. & Kaas, J.H. (1980). Projections from the medial nucleus of the inferior pulvinar complex to the middle temporal area of visual cortex. Neuroscience 5, 22192228.CrossRefGoogle Scholar
LIN, C.-S., Weller, R.E. & Kaas, J.H. (1982). Cortical connections of striate cortex in the owl monkey. Journal of Comparative Neurology 211, 165176.CrossRefGoogle ScholarPubMed
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 tracer study. Experimental Brain Research 69, 651661.CrossRefGoogle Scholar
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
Maunsell, J.H.R. & Van Essen, D.C. (1987). Topographic organization of the middle temporal visual area in the macaque monkey: Representational biases and the relationship to callosal connections and myeloarchitectonic boundaries. Journal of Comparative Neurology 266, 535555.CrossRefGoogle ScholarPubMed
Maunsell, J.H.R., Nealey, T.A. & Depriest, D.D. (1990). Magnocellular and parvocellular contributions to responses in the middle temporal visual area (MT) of the macaque monkey. Journal of Neuroscience 10, 33223334.CrossRefGoogle ScholarPubMed
Montero, V.M. (1980). Patterns of connections from the striate cortex to cortical visual areas in superior temporal sulcus of macaque and middle temporal gyrus of owl monkey. Journal of Comparative Neurology 189, 4555.CrossRefGoogle ScholarPubMed
Movshon, J.A. & Newsome, W.T. (1984). Functional characteristics of striate cortical neurons projecting to MT in the macaque. Neuroscience Abstracts 10, 933.Google Scholar
Rocha-Miranda, C., Bender, D., Gross, G.G. & Mlshkin, M. (1975). Visual activation of neurons in inferotemporal cortex depends on striate cortex and the forebrain commissure. Journal of Neurophysiology 38, 475491.CrossRefGoogle Scholar
Rodman, H.R., Gross, C.G. & Albright, T.D. (1989). Afferent basis of visual response properties in area MT of the macaque: I. Effects of striate cortex removal. Journal of Neuroscience 9, 20332050.CrossRefGoogle ScholarPubMed
Rodman, H.R., Gross, C.G. & Albright, T.D. (1990). Afferent basis of visual response properties in area MT of the macaque. II. Effects of superior colliculus removal. Journal of Neuroscience 10, 11541164.CrossRefGoogle ScholarPubMed
Schiller, P.H. & Malpeli, J.G. (1977). The effect of striate cortex cooling on area 18 cells in the monkey. Brain Research 126, 366369.CrossRefGoogle ScholarPubMed
Shipp, S. & Zeki, S. (1989). The organization of connections between areas V2 and V5 of macaque monkey visual cortex. European Journal of Neuroscience 1, 333354.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. (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. & Miskin, M. (1984). Subcortical projections of area MT in the macaque. Journal of Comparative Neurology 223, 368386.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
Wagor, E., Lin, C.S. & Kaas, J.H. (1975). Some cortical projections of the dorsomedial visual area (DM) of association cortex in the owl monkey, Aotus trivirgatus. Journal of Comparative Neurology 163, 227250.CrossRefGoogle ScholarPubMed
Weller, R.E. & Kaas, J.H. (1983). Retinotopic patterns of connections of area 17 with visual areas V-II and MT in macaque monkeys. Journal of Comparative Neurology 220, 253279.CrossRefGoogle ScholarPubMed
Weller, R.E. & Kaas, J.H. (1985). Cortical projections of the dorsolateral visual area in owl monkeys: The prestriate relay to inferior temporal cortex. Journal of Comparative Neurology 234, 3559.CrossRefGoogle ScholarPubMed
Weller, R.E., Wall, J.T. & Kaas, J.H. (1984). Cortical connections of the middle temporal visual area (MT) and the superior temporal cortex in owl monkeys. Journal of Comparative Neurology 228, 81104.CrossRefGoogle ScholarPubMed
Yukie, M. & Iwai, E. (1981). Direct projection from dorsal lateral geniculate nucleus to the prestriate cortex in macaque monkey. Journal of Comparative Neurology 201, 8198.CrossRefGoogle Scholar