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Oculomotor localization relies on a damped representation of saccadic eye displacement in human and nonhuman primates

Published online by Cambridge University Press:  02 June 2009

Paul Dassonville
Affiliation:
Brain Research Institute and Department of Anatomy and Cell Biology, University of California, Los Angeles
John Schlag
Affiliation:
Brain Research Institute and Department of Anatomy and Cell Biology, University of California, Los Angeles
Madeleine Schlag-Rey
Affiliation:
Brain Research Institute and Department of Anatomy and Cell Biology, University of California, Los Angeles

Abstract

The oculomotor system has long been thought to rely on an accurate representation of eye displacement or position in a successful attempt to reconcile a stationary target's retinal instability (caused by motion of the eyes) with its corresponding spatial invariance. This is in stark contrast to perceptual localization, which has been shown to rely on a sluggish representation of eye displacement, achieving only partial compensation for the retinal displacement caused by saccadic eye movements. Recent studies, however, have begun to cast doubt on the belief that the oculomotor system posseses a signal of eye displacement superior to that of the perceptual system. To verify this, five humans and one monkey (Macaca nemesthna) served as subjects in this study of oculomotor localization abilities. Subjects were instructed to make eye movements, as accurately as possible, to the locations of three successive visual stimuli. Presentation of the third stimulus (2-ms duration) was timed so that it fell before, during, or after the subject's saccade from the first stimulus to the second. Localization errors in each subject (human and nonhuman) were consistent with the hypothesis that the oculomotor system has access to only a damped representation of eye displacement —a representation similar to that found in perceptual localization studies.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1992

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References

Becker, W. & Jürgens, R. (1979). An analysis of the saccadic system by means of double step stimuli. Vision Research 19, 967983.CrossRefGoogle ScholarPubMed
Bischof, N. & Kramer, E. (1968). Untersuchungen and Überlegungen zur Richtungswahrnehmung bei willkürlichen sakkadischen Augenbewegungen. Psychologische Forschung 32, 185218.CrossRefGoogle Scholar
Boch, R., Fischer, B. & Ramsperger, E. (1984). Express-saccades of the monkey: Reaction times versus intensity, size, duration, and eccentricity of their targets. Experimental Brain Research 55, 223231.CrossRefGoogle ScholarPubMed
Bridgeman, B., Lewis, S., Heit, G. & Nagle, M. (1979). Relation between cognitive and motor-oriented systems of visual position perception. Journal of Experimental Psychology: Human Perception and Performance 5, 692700.Google ScholarPubMed
Dassonville, P., Schlag, J. & Schlag-Rey, M. (1992). The frontal eye field provides the goal of saccadic eye movement. Experimental Brain Research (in press).CrossRefGoogle Scholar
Dassonville, P., Schlag, J. & Schlag-Rey, M. (1900a). A damped representation of eye position is used in oculomotor localization. Society for Neuroscience Abstracts 16, 1085.Google Scholar
Dassonville, P., Schlag, J. & Schlag-Rey, M. (1990b). Time course of internal representation of eye position as derived from microstimulation experiments. Investigative Ophthalmology and Visual Science (Suppl.) 31, 84.Google Scholar
Dassonville, P., Schlag, J. & Schlag-Rey, M. (1991). Human oculomotor system uses both exoand egocentric cues in the localization of successive targets. Society for Neuroscience Abstracts 17, 860.Google Scholar
Fehrer, E. & Biederman, I. (1962). A comparison of reaction time and verbal report in the detection of masked stimuli. Journal of Experimental Psychology 64, 126130.CrossRefGoogle ScholarPubMed
Findlay, J.M. (1982). Global visual processing for saccadic eye movements. Vision Research 22, 10331045.CrossRefGoogle ScholarPubMed
Gnadt, J.W., Bracewell, R.M. & Andersen, R.A. (1991). Sensorimotor transformation during eye movements to remembered visual targets. Visual Research 31, 693715.Google ScholarPubMed
Gresty, M. & Leech, J. (1976). The assessment of position of stationary targets perceived during saccadic eye movements. Pflügers Archiv 366, 8388.Google Scholar
Grüsser, O.-J., Krizič, A. & Weiss, L.-R. (1987). Afterimage movement during saccades in the dark. Vision Research 27, 215226.CrossRefGoogle ScholarPubMed
Hallett, P.E. (1976). Saccades to flashes. In Eye Movements and Psychological Processes, ed. Monty, R.A. & Senders, J.W., pp. 255262. Hillsdale: Erlbaum.Google Scholar
Hallett, P.E. & Lightstone, A.D. (1976a). Saccadic eye movements towards stimuli triggered by prior saccades. Vision Research 16, 99106.CrossRefGoogle ScholarPubMed
Hallett, P.E. & Lightstone, A.D. (1976b). Saccadic eye movements to flashed targets. Vision Research 16, 107114.CrossRefGoogle ScholarPubMed
Hansen, R.M. & Skavenski, A.A. (1985). Accuracy of spatial localizations near the time of saccadic eye movements. Vision Research 25, 10771082.CrossRefGoogle ScholarPubMed
Hayhoe, M., Moeller, P., Ballard, D. & Albano, J.E. (1990). Guidance of saccades to remembered targets and the perception of spatial position. Investigative Ophthalmology and Visual Science (Suppl.) 31, 603.Google Scholar
Hershberger, W. (1987). Saccadic eye movements and the perception of visual direction. Perception and Psychophysics 41, 3544.CrossRefGoogle ScholarPubMed
Honda, H. (1989). Perceptual localization of visual stimuli flashed during saccades. Perception and Psychophysics 45, 162174.CrossRefGoogle ScholarPubMed
Honda, H. (1990). Eye movements to a visual stimulus flashed before, during, or after a saccade. In Attention and Performance XIII: Motor Representation and Control, ed. Jeannerod, M., pp. 567582. Hillsdale, NJ: Erlbaum.Google Scholar
Honda, H. (1991). The time courses of visual mislocalization and of extraretinal eye position signals at the time of vertical saccades. Vision Research 31, 19151921.CrossRefGoogle ScholarPubMed
Howard, I.P. (1982). Human Visual Orientation. Chichester, New York: John Wiley & Sons.Google Scholar
Judge, S.J., Richmond, B.J. & Chu, F.C. (1980). Implantation of magnetic search coils for measurement of eye position: An improved method. Vision Research 20, 535538.CrossRefGoogle ScholarPubMed
Kennard, D.W., Hartmann, R.W., Kraft, D.P. & Glaser, G.H. (1971). Brief conceptual (nonreal) events during eye movement. Biological Psychiatry 3, 205215.Google ScholarPubMed
Mateeff, S. (1978). Saccadic eye movements and localization of visual stimuli. Perception and Psychophysics 24, 215224.CrossRefGoogle ScholarPubMed
Matin, L. & Pearce, D.G. (1965). Visual perception of direction for stimuli flashed during voluntary saccadic eye movement. Science 148, 14851488.CrossRefGoogle Scholar
Miller, J.M. (1989). Egocentric localization around the time of saccadic eye movements. Investigative Ophthalmology and Visual Science (Suppl.) 30, 516.Google Scholar
Monahan, J.S. (1972). Extraretinal feedback and visual localization. Perception and Psychophysics 12, 349353.CrossRefGoogle Scholar
Pöppel, E., Held, R. & Frost, D. (1973). Residual visual function after brain wounds involving the central visual pathways in man. Nature 243, 295296.CrossRefGoogle ScholarPubMed
Robinson, D.A. (1963). A method of measuring eye movement using a scleral search coil in a magnetic field. IEEE Transactions on Biomedical Engineering 10, 137145.Google ScholarPubMed
Robinson, D.A. (1973). Models of the saccadic eye movement control system. Kybernetik 14, 7183.CrossRefGoogle ScholarPubMed
Robinson, D.A. (1975). Oculomotor control signals. In Basic Mechanisms of Ocular Motility and Their Clinical Implications, ed. Lennerstrand, G. & Bach-Y-Rita, P., pp. 337392. Oxford: Pergamon Press.Google Scholar
Robinson, D.A. (1981). Control of eye movements. In The Nervous System, Handbook of Physiology, Volume II, Part 2, ed. Brooks, V.B., pp. 12751320. Baltimore, Maryland: Williams and Wilkins.Google Scholar
Schlag, J., Schlag-Rey, M. & Dassonville, P. (1989). Interactions between natural and electrically evoked saccades. II. At what time is eye position sampled as a reference for the localization of a target? Experimental Brain Research 76, 548558.CrossRefGoogle ScholarPubMed
Schlag, J., Schlag-Rey, M. & Dassonville, P. (1990). Saccades can be aimed at the spatial location of targets flashed during pursuit. Journal of Neurophysiology 64, 575581.CrossRefGoogle ScholarPubMed
Schlag, J., Schlag-Rey, M. & Dassonville, P. (1991). Spatial programming of eye movements. In Brain and Space, ed. Paillard, J., pp. 7078. Oxford: Oxford University Press.CrossRefGoogle Scholar
Skavenski, A.A. (1990). Eye movement and visual localization of objects in space. In Reviews of Oculomotor Research, Volume 4: Eye Movements and Their Role in Visual and Cognitive Processes, ed. Kowler, E., pp. 263287. Amsterdam: Elsevier.Google Scholar
Skavenski, A.A. & Hansen, R.M. (1978). Role of eye position information in visual space perception. In Eye Movements and the Higher Psychological Functions, ed. Senders, J.W., Fisher, D.F. & Monty, R.A., pp. 1534. Hillsdale, NJ: Erlbaum.Google Scholar
Sparks, D.L., Mays, L.E. & Porter, J.D. (1987). Eye movements induced by pontine stimulation: Interaction with visually triggered saccades. Journal of Neurophysiology 58, 300318.CrossRefGoogle ScholarPubMed
Stanford, T.R., Carney, L.H. & Sparks, D.L. (1990). The amplitude of visually guided saccades is specified gradually in humans. Society for Neuroscience Abstracts 16, 901.Google Scholar