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Initial tracking conditions modulate the gain of visuo-motor transmission for smooth pursuit eye movements in monkeys

Published online by Cambridge University Press:  02 June 2009

Joshua D. Schwartz  and
Stephen G. Lisberger
Joshua D. Schwartz
Affiliation:
Department of Physiology, W.M. Keck Foundation Center for Integrative Neuroscience, and Neuroscience Graduate Program, University of California School of Medicine, San Francisco
Stephen G. Lisberger
Affiliation:
Department of Physiology, W.M. Keck Foundation Center for Integrative Neuroscience, and Neuroscience Graduate Program, University of California School of Medicine, San Francisco
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Abstract

Smooth pursuit eye movements allow primates to keep gaze pointed at small objects moving across stationary surroundings. In monkeys trained to track a small moving target, we have injected brief perturbations of target motion under different initial conditions as probes to read out the state of the visuo-motor pathways that guide pursuit. A large eye movement response was evoked if the perturbation was applied to a moving target the monkey was tracking. A small response was evoked if the same perturbation was applied to a stationary target the monkey was fixating. The gain of the response to the perturbation increased as a function of the initial speed of target motion and as a function of the interval from the onset of target motion to the time of the perturbation. The response to the perturbation also was direction selective. Gain was largest if the perturbation was along the axis of ongoing target motion and smallest if the perturbation was orthogonal to the axis of target motion. We suggest that two parallel sets of visual motion pathways through the extrastriate visual cortex may mediate, respectively, the visuo-motor processing for pursuit and the modulation of the gain of transmission through those pathways.

Keywords

Smooth pursuitVisual motionEye movementsAlert rhesus monkeySensory-motor processing
Type
Research Articles
Information
Visual Neuroscience , Volume 11 , Issue 3 , May 1994 , pp. 411 - 424
Copyright
Copyright © Cambridge University Press 1994

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References

Allman, J., Miezin, F. & McGuinness, E. (1985). Direction- and velocity-specific responses from beyond the classical receptive field in the middle temporal visual area (MT). Perception 14, 105–126.CrossRefGoogle ScholarPubMed
Brodal, P. (1978). The corticopontine projection in the rhesus monkey: Origin and principles of organization. Brain 101, 251–283.CrossRefGoogle ScholarPubMed
Brodal, P. (1979). The pontocerebellar projection in the rhesus monkey: An experimental study with retrograde axonal transport of horseradish peroxidase. Neuroscience 4, 193–208.CrossRefGoogle ScholarPubMed
Brodal, P. (1982). Further observations on the cerebellar projections from the pontine nucleus and the nucleus reticularis pontis in the rhesus monkey. Journal of Comparative Neurology 204, 44–55.CrossRefGoogle ScholarPubMed
Bruce, C.J., Goldberg, M.E., Bushnell, M.C. & Stanton, G.B. (1985). Primate frontal eye fields. II. Physiological and anatomical correlates of electrically evoked eye movements. Journal of Neurophysiology 54, 714–734.CrossRefGoogle ScholarPubMed
Dursteler, M.R. & Wurtz, R.H. (1988). Pursuit and optokinetic deficits following chemical lesions of cortical areas MT and MST. Journal of Neurophysiology 60, 940–965.CrossRefGoogle ScholarPubMed
Dursteler, 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, 1262–1287.CrossRefGoogle ScholarPubMed
Fries, W. (1981). The projection from striate and prestriate visual cortex onto the pontine nuclei in the macaque monkey. Society for Neuroscience Abstracts 7, 762.Google Scholar
Gerrits, N.M. & Voogd, J. (1989). The topographical organization of climbing and mossy fiber afferents in the flocculus and ventral para-flocculus in the rabbit, cat, and monkey. Experimental Brain Research (Suppl.) 17, 26–29.Google Scholar
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, 209–229.CrossRefGoogle ScholarPubMed
Glickstein, M., May, J. & Mercer, 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, 343–359.CrossRefGoogle ScholarPubMed
Goldreich, D., Krauzlis, R.J. & Lisberger, S.G. (1992). Effect of changing feedback delay on spontaneous oscillations in smooth pursuit eye movements of monkeys. Journal of Neurophysiology 67, 625–638.CrossRefGoogle ScholarPubMed
Grasse, K.L. & Lisberger, S.G. (1992). Analysis of a naturally occurring asymmetry in vertical smooth pursuit eye movement in a monkey. Journal of Neurophysiology 67, 164–179.CrossRefGoogle Scholar
Judge, S.G., Richmond, B.J. & Chu, F.C. (1980). Implantation of magnetic search coils for measurement of eye position. Vision Research 20, 535–538.CrossRefGoogle ScholarPubMed
Keating, E.G. (1991). Frontal eye field lesions impair predictive and visually-guided pursuit eye movements. Experimental Brain Research 86, 311–323.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, 31–47.CrossRefGoogle ScholarPubMed
Lisberger, S.G., Morris, E.J. & Tychsen, L. (1987). Visual motion processing and sensory-motor integration for smooth pursuit eye movements. Annual Review of Neuroscience 10, 97–129.CrossRefGoogle ScholarPubMed
Lisberger, S.G. & Westbrook, L.E. (1985). Properties of visual input that initiate horizontal smooth pursuit eye movements in monkeys. Journal of Neuroscience 5, 1662–1673.CrossRefGoogle ScholarPubMed
Luebke, A.E. & Robinson, D.A. (1988). Transition dynamics between pursuit and fixation suggest different systems. Vision Research 28, 941–946.CrossRefGoogle ScholarPubMed
Lynch, J.C. (1987). Frontal eye field lesions in monkeys disrupt pursuit. Experimental Brain Research 68, 437–441.CrossRefGoogle ScholarPubMed
MacAvoy, M.G., Gottlieb, J.P. & Bruce, C.J. (1991). Smooth pur-suit eye movement representation in the primate frontal eye field. Cerebral Cortex 1, 95–102.CrossRefGoogle ScholarPubMed
May, J.G., Keller, E.L. & Crandall, W.F. (1986). Changes in eye velocity during smooth pursuit tracking induced by microstimulation in the dorsolateral pontine nucleus of the macaque. Experimental Brain Research 63, 265–278.Google Scholar
McKee, S.P. (1981). A local mechanism for differential velocity detection. Vision Research 21, 491–500.CrossRefGoogle ScholarPubMed
Miles, F.A. & Eighmy, B.B. (1980). Long-term adaptive changes in the primate vestibulo-ocular reflex. I. Behavioral observations. Journal of Neurophysiology 43, 1406–1425.CrossRefGoogle Scholar
Morris, E.J. & Lisberger, S.G. (1987). Different responses to small visual errors during initiation and maintenance of smooth-pursuit eye movements in monkeys. Journal of Neurophysiology 58, 1351–1369.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 60, 664–686.CrossRefGoogle ScholarPubMed
Newsome, W.T., Wurtz, R.H., Dursteler, 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, 825–840.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, 604–620.CrossRefGoogle ScholarPubMed
Rashbass, C. (1961). The relationship between saccadic and smooth tracking eye movements. Journal of Physiology (London) 159, 326–338.CrossRefGoogle ScholarPubMed
Robinson, D. (1965). The mechanics of human smooth pursuit eye movement. Journal of Physiology (London) 180, 569–591.CrossRefGoogle ScholarPubMed
Robinson, D.A., Gordon, J.L. & Gordon, S.E. (1986). A model of the smooth pursuit eye movement system. Biological Cybernetics 55, 43–57.CrossRefGoogle Scholar
Stone, L.S. & Lisberger, S.G. (1990). Visual responses of Purkinje cells in the cerebellar flocculus during smooth-pursuit eye movements in monkeys. I. Simple spikes. Journal of Neurophysiology 63, 1241–1261.CrossRefGoogle ScholarPubMed
Suzuki, D.A. & Keller, E.L. (1984). Visual signals in the dorsolateral pontine nucleus of the alert monkey: Their relationship to smooth-pursuit eye movements. Experimental Brain Research 53, 473–478.CrossRefGoogle ScholarPubMed
Suzuki, D.A., May, J. & Keller, E.L. (1988). Smooth-pursuit eye movement deficits with chemical lesions in the dorsolateral pontine nucleus of the monkey. Journal of Neurophysiology 59, 952–977.Google Scholar
Thiers, P., Koehler, W. & Buettner, U.W. (1988). Neuronal activity in the dorsolateral pontine nucleus of the alert monkey modulated by visual stimuli and eye movements. Brain Research 72, 496–512.Google Scholar
Wurtz, R.H. (1969). Visual receptive fields of striate cortex neurons in awake monkeys. Journal of Neurophysiology 32, 727–742.CrossRefGoogle ScholarPubMed
Wurtz, R.H., Richmond, B.J. & Newsome, W.T. (1984). Modulation of cortical visual processing by attention. In Dynamic Aspects of Neocortical Function, ed. Edelman, G.M., Gall, W.E. & Cowan, W.M., p. 195. New York: Wiley.Google Scholar
Zee, D.S., Yamazaki, A., Butler, P.H. & Gucer, G. (1981). Effects of ablation of the flocculus and paraflocculus on eye movements in the primate. Journal of Neurophysiology 46, 878–899.CrossRefGoogle ScholarPubMed