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The effect of a moving distractor on the initiation of smooth-pursuit eye movements

Published online by Cambridge University Press:  02 June 2009

Vincent P. Ferrera  and
Stephen G. Lisberger
Vincent P. Ferrera
Affiliation:
University of California at San Francisco, Department of Physiology, W. M. Keck Foundation Center for Integrative Neuroscience, and Neuroscience Graduate Program, San Francisco
Stephen G. Lisberger
Affiliation:
University of California at San Francisco, Department of Physiology, W. M. Keck Foundation Center for Integrative Neuroscience, and Neuroscience Graduate Program, San Francisco
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Abstract

As a step toward understanding the mechanism by which targets are selected for smooth-pursuit eye movements, we examined the behavior of the pursuit system when monkeys were presented with two discrete moving visual targets. Two rhesus monkeys were trained to select a small moving target identified by its color in the presence of a moving distractor of another color. Smooth-pursuit eye movements were quantified in terms of the latency of the eye movement and the initial eye acceleration profile. We have previously shown that the latency of smooth pursuit, which is normally around 100 ms, can be extended to 150 ms or shortened to 85 ms depending on whether there is a distractor moving in the opposite or same direction, respectively, relative to the direction of the target. We have now measured this effect for a 360 deg range of distractor directions, and distractor speeds of 5–45 deg/s. We have also examined the effect of varying the spatial separation and temporal asynchrony between target and distractor. The results indicate that the effect of the distractor on the latency of pursuit depends on its direction of motion, and its spatial and temporal proximity to the target, but depends very little on the speed of the distractor. Furthermore, under the conditions of these experiments, the direction of the eye movement that is emitted in response to two competing moving stimuli is not a vectorial combination of the stimulus motions, but is solely determined by the direction of the target. The results are consistent with a competitive model for smooth-pursuit target selection and suggest that the competition takes place at a stage of the pursuit pathway that is between visual-motion processing and motor-response preparation.

Keywords

Smooth pursuitSensorimotor bottleneckCompetitive networksEye movementsVisual attentionMacaque
Type
Research Articles
Information
Visual Neuroscience , Volume 14 , Issue 2 , March 1997 , pp. 323 - 338
Copyright
Copyright © Cambridge University Press 1997

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References

REFERENCES

Albright, T.D. (1984). Direction and orientation selectivity of neurons in visual area MT of the macaque. Journal of Neurophysiology 52, 1106–1130.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.Google Scholar
Brodal, P. (1982). Further observation on the cerebellar projections from the pontine nucleus and the nucleus reticularis pontis in the rhesus monkey. Journal of Comparative Neurology 204, 44–55.Google Scholar
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
Duncan, J., Ward, R. & Shapiro, K. (1994). Direct measurement of attentional dwell time in human vision. Nature 369, 313–325.Google Scholar
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.Google Scholar
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
Ferrera, V.P. & Lisberger, S.G. (1995). Attention and target selection for smooth pursuit eye movements. Journal of Neuroscience 15, 7472–7484.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 paraflocculus 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.Google Scholar
Glickstein, M., Gerrits, N., Kralj-Hans, I., Mercier, B., Stein, J. & Voogd, J. (1994). Visual pontocerebellar projections in the macaque. Journal of Comparative Neurology 349, 51–72.Google Scholar
Glickstein, M., May, J., & Mercer, B.E. (1985). Corticopontine projection in the macaque: The distribution of labeled 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
Groh, J.M., Born, R.J. & Newsome, W.T. (1995). Microstimulation of area MT affects both saccades and smooth pursuit eye movements. Society for Neuroscience Abstracts 21, 281.Google Scholar
Heinen, S.J. (1995). Single neuron activity in the dorsomedial frontal cortex during smooth pursuit eye movements. Experimental Brain Research 104, 357–361.CrossRefGoogle ScholarPubMed
Huerta, M.F., Krubitzer, L.A. & Kaas, J.H. (1987). Frontal eye fields as defined by intracortical microstimulation in squirrel monkeys, owl monkeys and macaque monkeys. II. Cortical connections. Journal of Comparative Neurology 271, 473–492.Google Scholar
Hughes, H.C. & Zimba, L.D. (1987). Natural boundaries for the spatial spread of directed visual attention. Neuropsychologia 25, 5–18.Google Scholar
Judge, S.J., Richmond, B.J. & Chu, F.C. (1980). Implantation of magnetic search coils for measurement of eye position. Vision Research 20, 535–538.Google Scholar
Keating, E.G. (1991). Frontal eye field lesions impair predictive and visually-guided pursuit eye movements. Experimental Brain Research 86, 311–323.Google Scholar
Koch, C. & Ullman, S. (1985). Shifts in selective attention: towards the underlying neural circuitry. Human Neurobiology 4, 219–227.Google ScholarPubMed
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
Krauzlis, R.J. & Lisberger, S.G. (1991). Visual motion commands for pursuit eye movements in the cerebellum. Science 253, 568–571.CrossRefGoogle ScholarPubMed
Krauzlis, R.J. & Lisberger, S.G. (1994). Temporal properties of visual motion signals for the initiation of smooth pursuit eye movements in monkeys. Journal of Neurophysiology 72, 150–162.Google Scholar
Krubitzer, L.A. & Kaas, J.H. (1990). Cortical connections of MT in four species of primate: Areal, modular and retinotopic patterns. Visual Neuroscience 5, 165–204.CrossRefGoogle ScholarPubMed
Leichnetz, G.R. (1989). Inferior frontal eye field projections to the pursuitrelated dorsolateral pontine nucleus and middle temporal area (MT) in the monkey. Visual Neuroscience 3, 171–180.Google Scholar
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.Google Scholar
Lisberger, S.G. & Westbrook, L.E. (1985). Properties of visual inputs that initiate horizontal smooth pursuit eye movements in monkeys. Journal of Neuroscience 5, 1662–1673.Google Scholar
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-pursuit eye movement representation in the primate frontal eye field. Cerebral Cortex 1, 95–102.Google Scholar
Maioli, M.G., Squatrito, S., Galletti, C., Battaglini, P.P. & San-serverino, E.R. (1983). Corticocortical connections from the visual region of the superior temporal sulcus to frontal eye field in the macaque. Brain Research 265, 294–299.CrossRefGoogle ScholarPubMed
Maunsell, J.H.R. & Van Essen, D.C. (1983). Functional properties of neurons in the middle temporal visual area (MT) of the macaque monkey: I. Selectivity for stimulus direction, speed and orientation. Journal of Neurophysiology 49, 1127–1147.CrossRefGoogle ScholarPubMed
Meyer, C.H., Lasker, A.G. & Robinson, D.A. (1985). The upper limit of human smooth pursuit velocity. Vision Research 25, 561–563.Google Scholar
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
Moran, J. & Desimone, R. (1985). Selective attention gates visual processing in the extrastriate cortex. Science 229, 782–784.Google Scholar
Movshon, J.A., Lisberger, S.G. & Krauzlis, R.J. (1990). Visual cortical signals supporting smooth pursuit eye movements. Cold Spring Harbor Symposia on Quantitative Biology 55, 707–716.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
Preddie, D.C., Connor, C.E., Gallant, J.L. & Van Essen, D.C. (1995). Time course of attentional effects in macaque area V4. Society for Neuroscience Abstracts 21, 1759.Google Scholar
Rashbass, C. (1961). The relationship between saccadic and smooth tracking eye movements. Journal of Physiology 159, 326–338.Google Scholar
Robinson, F.R., Cohen, J.L., May, J., Sestokas, A.K. & Glickstein, M. (1984). Cerebellar targets of visual pontine cells in the cat. Journal of Comparative Neurology 223, 471–482.Google Scholar
Schall, J.D., Morel, A., King, D.J. & Bullier, J. (1995). Topography of visual cortex connections with frontal eye field in macaque: Convergence and segregation of processing streams. Journal of Neuroscience 15, 4464–4487.CrossRefGoogle ScholarPubMed
Stanton, G.B., Goldberg, M.E. & Bruce, C.J. (1988). Frontal eye field efferents in the macaque monkey: II. Topography of terminal fields in midbrain and pons. Journal of Comparative Neurology 271, 493–506.Google 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. (1988). Visual signals in the dorsolateral pontine nucleus of the alert monkey: Their relationship to smooth-pursuit eye movements. Experimental Brain Research 53, 473–478.Google Scholar
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
Thier, 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
Tipper, S.P. (1990). Early or late selection? Still an open question. Behavioral Brain Science 13, 255.Google Scholar
Ungerleider, L.G. & Desimone, R. (1986). Cortical connections of visual area MT in the macaque. Journal of Comparative Neurology 248, 190–222.Google Scholar
Westheimer, G. & Blair, M. (1973). Oculomotor deficits in cerebellectomized monkeys. Investigative Ophthalmology 12, 618–621.Google Scholar
Williams, D. & Phillips, G. (1987). Cooperative phenomena in the perception of motion direction. Journal of the Optical Society of America A 4, 878–885.Google Scholar
Williams, D., Phillips, G. & Sekuler, R. (1986). Hysteresis in the perception of motion direction as evidence for neural cooperativity. Nature 324, 253–255.CrossRefGoogle ScholarPubMed
Wilson, H.R. & Cowan, J.D. (1972). Excitatory and inhibitory interactions in localized populations of model neurons. Biophysical Journal 12, 1–24.Google Scholar
Wilson, H.R., Ferrera, V.P. & Yo, C. (1992). A psychophysically motivated model for two-dimensional motion perception. Visual Neuroscience 9, 79–91.Google Scholar
Wurtz, R.H. (1969). Visual receptive fields of striate cortex neurons in awake monkeys. Journal of Neurophysiology 32, 727–742.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.Google Scholar
Zivotofsky, A.Z., Averbuch-Heller, L., Thomas, C.W., Das, V.E., Discenna, A.O. & Leigh, R.J. (1995). Tracking of illusory target motion: Differences between gaze and head responses. Vision Research 35, 3029–3035.Google Scholar