Hostname: page-component-cd9895bd7-7cvxr Total loading time: 0 Render date: 2024-12-26T00:49:30.043Z Has data issue: false hasContentIssue false

Topography of eye-position sensitivity of saccades evoked electrically from the cat's superior colliculus

Published online by Cambridge University Press:  02 June 2009

James T. McIlwain
Affiliation:
Section of Neurobiology, Division of Biology and Medicine, Brown University, Providence

Abstract

Saccades evoked electrically from the deep layers of the superior colliculus have been examined in the alert cat with its head fixed. Amplitudes of the vertical and horizontal components varied linearly with the starting position of the eye. The slopes of the linear-regression lines provided an estimate of the sensitivity of these components to initial eye position. In observations on 29 sites in nine cats, the vertical and horizontal components of saccades evoked from a given site were rarely influenced to the same degree by initial eye position. For most sites, the horizontal component was more sensitive than the vertical component. Sensitivities of vertical and horizontal components were lowest near the representations of the horizontal and vertical meridians, respectively, of the collicular retinotopic map, but otherwise exhibited no systematic retinotopic dependence. Estimates of component amplitudes for saccades evoked from the center of the oculomotor range also diverged significantly from those predicted from the retinotopic map. The results of this and previous studies indicate that electrical stimulation of the cat's superior colliculus cannot yield a unique oculomotor map or one that is in register everywhere with the sensory retinotopic map. Several features of these observations suggest that electrical stimulation of the colliculus produces faulty activation of a saccadic control system that computes target position with respect to the head and that small and large saccades are controlled differently.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1990

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

Albano, J.E. & Wurtz, R.H. (1982). Deficits in eye position following ablation of monkey superior colliculus, pretectum, and posterior medial thalamus. Journal of Neurophysiology 48 318337.CrossRefGoogle ScholarPubMed
Antonini, A., Berlucchi, G. & Sprague, J.M. (1978). Indirect, across-the-midline retinotectal projections and representation of ipsilateral visual field in superior colliculus of cat. Journal of Neurophysiology 41, 285304.CrossRefGoogle ScholarPubMed
Becker, W. & JÜrgens, R. (1979). An analysis of the saccadic system by means of double-step stimuli. Vision Research 19, 967983.CrossRefGoogle ScholarPubMed
Berthoz, A., Grantyn, A. & Droulez, J. (1986). Some collicular efferent neurons code saccadic eye velocity. Neuroscience Letters 72, 289294.CrossRefGoogle ScholarPubMed
Blakemore, C. & Donaghy, M. (1980). Coordination of head and eyes in the gaze changing behavior of cats. Journal of Physiology 300, 317335.CrossRefGoogle ScholarPubMed
BÜttner, U. & BÜttner-Ennever, J.A. (1988). Present concepts of oculomotor organization. In Neuroanatomy of the Oculomotor System. Reviews in Oculomotor Research. Vol. 2, ed. Buttnerennever, J.A., pp. 232. Amsterdam: Elsevier.Google Scholar
Cohen, B., Matsuo, V., Fradin, J. & Lapham, T. (1985). Horizontal saccades induced by stimulation of the central mesencephalic reticular formation. Experimental Brain Research 57, 605616.CrossRefGoogle ScholarPubMed
Crommelinck, M., Roucoux, A. & Meulders, M. (1977). Eye movements evoked by stimulation of lateral posterior nucleus and pulvinar in the alert cat. Brain Research 124, 361366.CrossRefGoogle ScholarPubMed
Dixon, W.J. & Massey, F.J. Jr (1957). Introduction To Statistical Analysis, 2nd edition. New York: McGraw-Hill.CrossRefGoogle Scholar
Evinger, C., Kaneko, C.R.S. & Fuchs, A.F. (1981). Oblique saccadic eye movements of the cat. Experimental Brain Research 41, 370379.Google ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Fuchs, A.F., Kaneko, C.R.S. & Scudder, C.A. (1985). Brain-stem control of saccadic eye movements. Annual Review of Neuroscience 8, 307337.CrossRefGoogle ScholarPubMed
Godaux, E., Cheron, G. & Gravis, F. (1989). Eye movements evoked by microstimulations in the brain stem of the alert cat. Experimental Brain Research 77, 94102.CrossRefGoogle ScholarPubMed
Guitton, D. & Mandl, G. (1978). Frontal oculomotor area in alert cat, I: Eye movements and neck activity evoked by stimulation. Brain Research 149, 295312.CrossRefGoogle ScholarPubMed
Guitton, D., Crommelinck, M. & Roucoux, A. (1980). Stimulation of the superior colliculus in the alert cat, I: Eye movements and neck EMG activity evoked when the head is restrained. Experimental Brain Research 39, 6373.Google ScholarPubMed
Guitton, D., Douglas, R.M. & Volle, M. (1984). Eye-head coordination of cats. Journal of Neurophysiology 52, 10301050.CrossRefGoogle Scholar
Hikosaka, O. & Wurtz, R.H. (1985). Modification of saccadic eye movements by GABA-related substances, I: Effects of muscimol and bicuculline in monkey superior colliculus. Journal of Neurophysiology 53, 266291.CrossRefGoogle ScholarPubMed
Hyde, J.E. & Eason, R.G. (1959). Characteristics of ocular movements evoked by stimulation of brain stem of cat. Journal of Neurophysiology 22, 666678.CrossRefGoogle ScholarPubMed
Hyde, J.E. & Eliasson, S.G. (1957). Brainstem induced eye movements in cats. Journal of Comparative Neurology 108, 139172.CrossRefGoogle ScholarPubMed
Judge, S.T., Richmond, B.J. & Chiu, F.C. (1980). Implantation of magnetic search coils for measurement of eye position: an improved method. Vision Research 20, 535538.CrossRefGoogle ScholarPubMed
Kurylo, D.D. & Skavenski, A.A. (1987). Eye movements elicited by stimulation of the posterior parietal cortex in the monkey. Investigative Ophthalmology and Visual Science (Suppl.) 28, 333.Google Scholar
Lee, C., Rohrer, W.H. & Sparks, D.L. (1988). Population coding of saccadic eye movements by neurons in the superior colliculus. Nature 332, 357360.CrossRefGoogle ScholarPubMed
Maldonado, H., Joseph, J.-P. & Schlag, J. (1980). Types of eye movements evoked by thalamic microstimulation in the alert cat. Experimental Neurology 70, 613625.CrossRefGoogle ScholarPubMed
Mays, L.E. & Sparks, D.L. (1980). Saccades are spatially, not retinocentrically, coded. Science 208, 11631165.CrossRefGoogle Scholar
McElligott, J.G. & Keller, E.L. (1984). Cerebellar vermis involvement in monkey saccadic eye movements: microstimulation. Experimental Neurology 86, 543558.CrossRefGoogle ScholarPubMed
McIlwain, J.T. (1975). Visual receptive fields and their images in the superior colliculus of the cat. Journal of Neurophysiology 38, 219230.CrossRefGoogle ScholarPubMed
McIlwain, J.T. (1983). Representation of the visual streak in visuotopic maps of the cat's superior colliculus: influence of the mapping variable. Vision Research 23, 507516.CrossRefGoogle ScholarPubMed
McIlwain, J.T. (1986). Effects of eye position on saccades evoked electrically from superior colliculus of alert cats. Journal of Neurophysiology 55, 97112.CrossRefGoogle ScholarPubMed
McIlwain, J.T. (1988 a). Saccadic eye movements evoked by electrical stimulation of the cat's visual cortex. Visual Neuroscience 1, 135143.CrossRefGoogle ScholarPubMed
McIlwain, J.T. (1988 b). Effects of eye position on electrically evoked saccades: a theoretical note. Visual Neuroscience 1, 239244.CrossRefGoogle ScholarPubMed
Munoz, D. & Guitton, D. (1988). Rostral output neurons of superior colliculus are active during attentive fixation. Society for Neuroscience Abstracts 14, 956.Google Scholar
Ohtsuka, K., Edamura, M., Kawahara, K. & Aoki, M. (1987). The properties of goal-directed eye movements evoked by microstimulation of the cerebellar vermis in the cat. Neuroscience Letters 76, 173179.CrossRefGoogle ScholarPubMed
Pettigrew, J.D., Cooper, M.L. & Blasdel, G.G. (1979). Improved use of tapetal reflection for eye-position monitoring. Investigative Ophthalmology and Visual Science 18, 490495.Google 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. (1972). Eye movments evoked by collicular stimulation in the alert monkey. Vision Research 12, 17951808.CrossRefGoogle Scholar
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. 337374. Oxford, England: Pergamon Press.Google Scholar
Ron, S. & Robinson, D.A. (1973). Eye movements evoked by cerebellar stimulation in the alert monkey. Journal of Neurophysiology 36, 10041022.CrossRefGoogle ScholarPubMed
Roucoux, A. & Crommelinck, M. (1976). Eye movements evoked by superior colliculus stimulation in the alert cat. Brain Research 106, 349363.CrossRefGoogle ScholarPubMed
Roucoux, A., Guitton, D. & Crommelinck, M. (1980). Stimulation of the superior colliculus in the alert cat, II: Eye and head movements evoked when the head is unrestrained. Experimental Brain Research 39, 7585.CrossRefGoogle ScholarPubMed
Schlag-Rey, M., Schiag, J. & Shook, B. (1989). Interactions between natural and electrically evoked saccades, I: Differences between sites carrying retinal-error and motor-error signals in monkey superior colliculus. Experimental Brain Research 76, 537547.CrossRefGoogle ScholarPubMed
Scudder, C.A. (1988). A new local feedback model of the saccadic burst generator. Journal of Neurophysiology 59, 14551475.CrossRefGoogle ScholarPubMed
Segraves, M.A. & Goldberg, M.E. (1984). Initial orbital position affects the trajectories of large saccades evoked by electrical stimulation of the monkey superior colliclulus. Society for Neuroscience Abstracts 10, 389.Google Scholar
Sparks, D.L. (1986). Translation of sensory signals into commands for control of saccadic eye movements: role of primate superior colliculus. Physiological Reviews 66, 118171.CrossRefGoogle ScholarPubMed
Sparks, D.L., Holland, R. & Guthrie, B.L. (1976). Size and distribution of movement fields in the monkey superior colliculus. Brain Research 113, 2134.CrossRefGoogle ScholarPubMed
Straschill, M. & Rieger, P. (1973). Eye movements evoked by focal stimulation of the cat's superior colliculus. Brain Research 59, 211227.CrossRefGoogle ScholarPubMed
Van, Gisbergen J.A.M. & van, Opstal A.J. (1989). Models. In The Neurobiology of Saccadic Eye Movements. Reviews of Oculomotor Research, Vol. 3, ed. Wurtz, R.H. & Goldberg, M.E., pp. 69101. Amsterdam: Elsevier.Google Scholar
Van, Gisbergen J.A.M., van, Opstal A.J. & Tax, A.A.M. (1987). Collicular ensemble coding of saccades based on vector summation. Neuroscience 21, 541556.Google Scholar
Waitzman, D.M., Ma, T.P., Optican, L.M. & Wurtz, R.H. (1988). Superior colliculus neurons provide the saccadic motor error signal. Experimental Brain Research 72, 649652.CrossRefGoogle ScholarPubMed
Westheimer, G.E. & Blair, S.M. (1975). Synkinese der Augen- und Kopfbewegungen bei Hirnstammreizungen am wachen Macacus Affen. Experimental Brain Research 24, 8995.CrossRefGoogle Scholar