Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-24T01:53:27.430Z Has data issue: false hasContentIssue false

Endpoint accuracy in saccades interrupted by stimulation in the omnipause region in monkey

Published online by Cambridge University Press:  02 June 2009

E.L. Keller
Affiliation:
Smith-Kettlewell Eye Research Institute, 2232 Webster Street, San Francisco Department of Electrical Engineering and Computer Sciences, University of California, Berkeley Joint Graduate Program in Bioengineering, University of California, San Francisco and Berkeley
N.J. Gandhi
Affiliation:
Smith-Kettlewell Eye Research Institute, 2232 Webster Street, San Francisco Joint Graduate Program in Bioengineering, University of California, San Francisco and Berkeley
J.M. Shieh
Affiliation:
Smith-Kettlewell Eye Research Institute, 2232 Webster Street, San Francisco Department of Electrical Engineering and Computer Sciences, University of California, Berkeley

Abstract

Electrical stimulation of the omnipause neuron region (OPN) at saccade onset results in interrupted saccades (IS) —eye movements which pause in midflight, resume after a brief period, and end near the target location. Details on the endpoint accuracy of IS do not exist, except for a brief report by Becker et al. (1981). Their analysis emphasized the accuracy of IS relative to the visual target which remained on during the interrupted period. We instead quantified the metric properties of IS relative to nonstimulated saccades during a target flash paradigm. Our results show that IS tend to be slightly hypermetric relative to the nonstimulated saccades to the same target location. The amount of overshoot is not correlated with target eccentricity. Detailed analyses also indicate that the standard deviations of the endpoint in IS are not significantly larger than those for nonstimulated saccades, although there was a much larger variability produced in eye position during the interruption. Both these latter observations support the notion that saccades are controlled by an internal negative feedback system. Also, the size of the remaining motor error during the interrupted period is one factor influencing when an IS resumes, but the variability in this measure is large particularly for smaller motor errors. Recent results have suggested that the resettable neural integrator involved in the feedback loop may be reset after each saccade through an exponential decay process. To probe the properties of the neural integrator, we varied the duration of interruption between the initial and resumed saccades and sought a systematic overshoot in the final eye position with increasing interruption period and variable initial saccade size. Our results showed the neural integrator does not decay during the pause period of interrupted saccades.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1996

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

Becker, W., King, W.M., Fuchs, A.F., Jürgens, R., Johanson, G. & Kornhuber, H.H. (1981). Accuracy of goal-directed saccades and mechanisms of error correction. In Progress in Oculomotor Research, ed. Fuchs, A.F. & Becker, W., pp. 2937. New York: Elsevier.Google Scholar
Crandall, W.F. & Keller, E.L. (1985). Visual and oculomotor signals in nucleus reticularis tegmenti pontis in alert monkey. Journal of Neurophysiology 54, 13261345.Google Scholar
Fuchs, A.F. & Robinson, D.A. (1966). A method for measuring horizontal and vertical eye movement chronically in the monkey. Journal of Applied Physiology 21, 10681070.Google Scholar
Gandhi, N.J. & Keller, E.L. (1995). Interrupting saccades by electrical stimulation of the superior colliculus determines an extended fixation zone. Society for Neuroscience Abstracts 21, 1193.Google Scholar
Gandhi, N.J., Keller, E.L. & Hartz, K.E. (1994). Interpreting the role of collicular buildup neurons in saccadic eye movement control. Society for Neuroscience Abstracts 20, 141.Google Scholar
Judge, S.J., Richmond, B.J. & Chu, F.C. (1980). Implantations of magnetic search coils for measurement of eye position: An improved method. Vision Research 20, 535538.Google Scholar
Keller, E.L. (1974). Participation of the medial pontine reticular formation in eye movement generation in monkey. Journal of Neurophysiology 37, 316332.Google Scholar
Keller, E.L. (1977). Control of saccadic eye movements by midline brain stem neurons. In Control of Gaze by Brain Stem Neurons, ed. Baker, R. & Berthoz, A., pp. 327336. Amsterdam: Elsevier.Google Scholar
Keller, E.L. & Edelman, J.A. (1994). Use of interrupted saccade paradigm to study spatial and temporal dynamics of saccadic burst cells in superior colliculus in monkey. Journal of Neurophysiology 72, 27542770.CrossRefGoogle ScholarPubMed
King, W.M. & Fuchs, A.F. (1977). Neuronal activity in the mesencephalon related to vertical eye movements. In Control of Gaze by Brain Stem Neurons, ed. Baker, R. & Berthoz, A., pp. 319326. Amsterdam: Elsevier.Google Scholar
Kustov, A.A. & Robinson, D.L. (1995). Modified saccades evoked by stimulation of the macaque superior colliculus account of properties of the resettable integrator. Journal of Neurophysiology 73, 17241728.CrossRefGoogle ScholarPubMed
Moschovakis, A.K. & Highstein, S.M. (1994). The anatomy and physiology of primate neurons that control rapid eye movements. Annual Review of Neuroscience 17, 465488.Google Scholar
Munoz, O.P. & Wurtz, R.H. (1993). Fixation cells in monkey superior colliculus II. Reversible activation and deactivation. Journal of Neurophysiology 70, 576589.Google Scholar
Nichols, M.J. & Sparks, D.L. (1995). Nonstationary properties of the saccadic system: New constraints on models of saccadic control. Journal of Neurophysiology 73, 431435.CrossRefGoogle ScholarPubMed
Paré, M. & Guitton, D. (1994). The fixation area of the cat superior colliculus: Effects of electrical stimulation and direct connection with brainstem omnipause neurons. Experimental Brain Research 101, 109122.CrossRefGoogle ScholarPubMed
Pélisson, D., Guitton, D. & Goffart, L. (1995). On-line compensation of gaze shifts perturbed by micro-stimulation of the superior colliculus in the cat with unrestrained head. Experimental Brain Research 106, 196204.Google Scholar
Robinson, D.A. (1963). A method of measuring eye movement using a scierai search coil in a magnetic field. IEEE Transactions on Biomedical Engineering BME-10, 137145.Google Scholar
Robinson, D.A. (1972). Eye movements evoked by collicular stimulation in the alert monkey. Vision Research 12, 17951808.CrossRefGoogle ScholarPubMed
Robinson, D.A. (1975). Oculomotor control signals. In Basic Mechanisms of Ocular Motilily and Their Clinical Implications, ed. Lennerstrand, G. & Bach-Y-Rita, P., pp. 337374. Oxford, England: Pergamon Press.Google Scholar
Scudder, C.A. (1988). A new local feedback model of the saccadic burst generator. Journal of Neurophysiology 59, 14551475.Google Scholar
Van Gisbergen, J.A.M., Robinson, D.A. & Gielen, S. (1981). A quantitative analysis of generation of saccadic eye movements by burst neurons. Journal of Neurophysiology 45, 417442.Google Scholar
Van Opstal, A.J., & Van Gisbergen, J.A.M. (1990). Role of monkey superior colliculus in saccade averaging. Experimental Brain Research 79, 143149.Google Scholar