Hostname: page-component-848d4c4894-nmvwc Total loading time: 0 Render date: 2024-07-07T17:30:58.842Z Has data issue: false hasContentIssue false
  • English
  • Français

Distributed spatial coding in the superior colliculus: A review

Published online by Cambridge University Press:  02 June 2009

James T. McIlwain
James T. McIlwain
Affiliation:
Division of Biology and Medicine, Brown University, Providence
Get access Rights & Permissions [Opens in a new window]

Abstract

This paper reviews evidence that the superior colliculus (SC) of the midbrain represents visual direction and certain aspects of saccadic eye movements in the distribution of activity across a population of cells. Accurate and precise eye movements appear to be mediated, in part at least, by cells of the SC that have large sensory receptive fields and/or discharge in association with a range of saccades. This implies that visual points or saccade targets are represented by patches rather than points of activity in the SC. Perturbation of the pattern of collicular discharge by focal inactivation modifies saccade amplitude and direction in a way consistent with distributed coding. Several models have been advanced to explain how such a code might be implemented in the colliculus. Evidence related to these hypotheses is examined and continuing uncertainties are identified.

Keywords

Superior colliculusSaccadeDistributed codingEnsemble codingPopulation coding
Type
Research Article
Information
Visual Neuroscience , Volume 6 , Issue 1 , January 1991 , pp. 3 - 13
Copyright
Copyright © Cambridge University Press 1991

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

Albus, K. (1975). A quantitative study of the projection area of the central and precentral visual field in area 17 of the cat, I: Precision of the topography. Experimental Brain Research 24, 159–179.CrossRefGoogle Scholar
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, 285–304.CrossRefGoogle ScholarPubMed
Appell, P.P. & Behan, M. (1990). Sources of subcortical GABAergic projections to the superior colliculus in the cat. Journal of Comparative Neurology (in press).CrossRefGoogle Scholar
Apter, J. (1946 a). Projection of the retina on superior colliculus of cats. Journal of Neurophysiology 8, 123–134.CrossRefGoogle Scholar
Apter, J.T. (1946 b). Eye movements following strychninization of the superior colliculus of cats. Journal of Neurophysiology 9, 73–86.CrossRefGoogle ScholarPubMed
Becker, W. & Jürgens, R. (1979). An analysis of the saccadic system by means of double-step stimuli. Vision Research 19, 967–983.CrossRefGoogle ScholarPubMed
Behan, M. (1985). An EM-autoradiographic and EM-HRP study of the commissural projection of the superior colliculus in the cat. Journal of Comparative Neurology 234, 105–116.CrossRefGoogle ScholarPubMed
Berthoz, A., Grantyn, A. & Droulez, J. (1986). Some collicular efferent neurons code saccadic eye velocity. Neuroscience Letters 72, 289–294.CrossRefGoogle ScholarPubMed
Blakemore, C. & Donaghy, M. (1980). Coordination of head and eyes in the gaze changing behavior of cats. Journal of Physiology 300, 317–335.CrossRefGoogle ScholarPubMed
Capuano, U. & McIlwain, J.T. (1981). Reciprocity of receptive-field images and point images in the superior colliculus of the cat. Journal of Comparative Neurology 196, 13–23.CrossRefGoogle ScholarPubMed
Chalupa, L.M. & Rhoades, R.W. (1977). Responses of visual, somatosensory, and auditory neurones in the golden hamster's superior colliculus. Journal of Physiology 270, 595–626.CrossRefGoogle ScholarPubMed
Cohen, B. & Büttner-Ennever, J.A. (1984). Projections from the superior colliculus to a region of the central mesencephalic reticular formation (cMRF) associated with horizontal saccadic eye movements. Experimental Brain Research 57, 167–176.CrossRefGoogle ScholarPubMed
Cohen, B., Matsuo, V., Fradin, J. & Lapham, T. (1985). Horizontal saccades induced by stimulation of the central mesencephalic reticular formation. Experimental Brain Research 57, 605–616.CrossRefGoogle ScholarPubMed
Cynader, M. & Berman, N. (1972). Receptive-field organization of monkey superior colliculus. Journal of Neurophysiology 35, 187–201.CrossRefGoogle ScholarPubMed
Dean, P., Redgrave, P. & Westby, G.W.M. (1989). Event or emergency? Two response systems in the mammalian superior colliculus. Trends in Neurosciences 12, 137–147.CrossRefGoogle ScholarPubMed
Douglas, R.M. & Vetter, M. (1986). Widespread inhibition and target selection in the superior colliculus. Society for Neuroscience Abstracts 12, 458.Google Scholar
Dow, B.M., Snyder, A.Z., Vautin, R.G. & Bauer, R. (1981). Magnification factor and receptive-field size in foveal striate cortex of the monkey. Experimental Brain Research 44, 213–228.CrossRefGoogle ScholarPubMed
Dräger, U.C. & Hubel, D.H. (1975). Responses to visual stimulation and relationship between visual, auditory, and somatosensory inputs in mouse superior colliculus. Journal of Neurophysiology 38, 690–713.CrossRefGoogle ScholarPubMed
Du Lac, S. & Knudsen, E.I. (1987). The optic tectum encodes saccade magnitude in a push-pull fashion in the barn owl. Society for Neuroscience Abstracts 13, 393.Google Scholar
Edwards, S.B. (1977). The commissural projection of the superior colliculus in the cat. Journal of Comparative Neurology 173, 23–40.CrossRefGoogle ScholarPubMed
Edwards, S.B. & Henkel, C.K. (1978). Superior colliculus connections with the extraocular motor nuclei in the cat. Journal of Comparative Neurology 179, 451–468.CrossRefGoogle ScholarPubMed
Edwards, S.B., Ginsburgh, C.L., Henkel, C.K. & Stein, B.E. (1979). Sources of subcortical projections to the superior colliculus in the cat. Journal of Comparative Neurology 184, 309–330.CrossRefGoogle Scholar
Erickson, R.P. (1968). Stimulus coding in topographic and non-topographic afferent modalities. Psychological Reviews 75, 447–465.CrossRefGoogle Scholar
Erickson, R.P. (1974). Parallel “population” neural coding in feature extraction. In The Neurosciences. Third Study Program, ed. Schmitt, F.O. & Worden, F.G., pp. 155–169. Cambridge: MIT.Google Scholar
Findlay, J.M. (1982). Global visual processing for saccadic eye movements. Vision Research 22, 1033–1045.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, 307–337.CrossRefGoogle ScholarPubMed
Gielen, C.C.A.M. & Van Gisbergen, J.A.M. (1990). The visual guidance of saccades and fast aiming movements. News in Physiological Sciences 5, 58–63.Google Scholar
Goldberg, M.E. & Wurtz, R.H. (1972). Activity of superior colliculus in behaving monkey, I: Visual receptive fields of single neurons. Journal of Neurophysiology 35, 542–559.CrossRefGoogle ScholarPubMed
Gordon, B. (1973). Receptive fields in deep layers of cat superior colliculus. Journal of Neurophysiology 36, 157–178.CrossRefGoogle ScholarPubMed
Graham, J. (1977). An autoradiographic study of the efferent connections of the superior colliculus of the cat. Journal of Comparative Neurology 173, 629–654.CrossRefGoogle ScholarPubMed
Grantyn, R. (1988). Gaze control through the superior colliculus: structure and function. In Neuroanatomy of the Oculomotor System. Reviews in Oculomotor Research, Vol. 2, ed. Büttner-Ennever, J., pp. 273–334. Amsterdam: Elsevier.Google Scholar
Grantyn, A. & Grantyn, R. (1982). Axonal patterns and sites of termination of cat superior colliculus neurons projecting in the tectobulbo-spinal tract. Experimental Brain Research 46, 243–256.CrossRefGoogle ScholarPubMed
Grobstein, P. (1988). Between the retinotectal projection and directed movement: topography of a sensorimotor interface. Brain, Behavior, and Evolution 31, 34–48.CrossRefGoogle ScholarPubMed
Guitton, D., Crommelink, 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, 63–73.Google ScholarPubMed
Guitton, D., Douglas, R.M. & Volle, M. (1984). Eye-head coordination in cats. Journal of Neurophysiology 52, 1030–1050.CrossRefGoogle ScholarPubMed
Guitton, D., Munoz, D.P. & Galiana, H.L. (1990). Gaze control in the cat: studies and modeling of the coupling between orienting eye and head movements in different behavioral tasks. Journal of Neurophysiology 64, 509–531.CrossRefGoogle ScholarPubMed
Harris, L.R. (1980). The superior colliculus and movements of the head and eyes in cats. Journal of Physiology 300, 367–392.CrossRefGoogle ScholarPubMed
Harting, J.K. (1977). Descending pathways from the superior colliculus: an autoradiographic analysis in the rhesus monkey (Macaca mulatta). Journal of Comparative Neurology 173, 583–612.CrossRefGoogle ScholarPubMed
Harting, J.K., Huerta, M., Hashikawa, T., Weber, J. & Van Lieshout, D.P. (1988). Neuroanatomical studies of the nigrotectal projection in the cat. Journal of Comparative Neurology 278, 615–632.CrossRefGoogle ScholarPubMed
Heggelund, P. & Albus, K. (1978). Response variability and orientation discrimination of single cells in striate cortex of cat. Experimental Brain Research 32, 197–212.CrossRefGoogle ScholarPubMed
Henn, V. & Cohen, B. (1976). Coding of information about rapid eye movements in the pontine reticular formation of alert monkeys. Brain Research 108, 307–325.CrossRefGoogle ScholarPubMed
Hepp, K. & Henn, V. (1983). Spatio-temporal recoding of rapid eye movement signals in the monkey paramedian pontine reticular formation. Experimental Brain Research 52, 105–120.CrossRefGoogle ScholarPubMed
Hikosaka, O. & Wurtz, R.H. (1986). Saccadic eye movements following injection of lidocaine into the superior colliculus. Experimental Brain Research 61, 531–539.CrossRefGoogle ScholarPubMed
Hinton, G.H., McClelland, J.L. & Rumelhart, D.E. (1985). Distributed representations. In Parallel Distributed Processing: Explorations in the Microstructure of Cognition, Vol. 1, ed. Rumelhart, D.E. & McClelland, J.L., pp. 77–109. Cambridge: Bradford.Google Scholar
Hirsch, J.A., Chan, J.C.K. & Yin, T.C.T. (1985). Responses of neurons in the cat's superior colliculus to acoustic stimuli, I: Monaural and binaural response properties. Journal of Neurophysiology 53, 726–745.CrossRefGoogle ScholarPubMed
Hoffmann, K.-P. (1970). Retinotopische Beziehungen und Strucktur rezeptiver Felder in Tectum Opticum und Praetectum der Katze. Zeitschrift für Vergleichende Physiologie 67, 26–57.CrossRefGoogle Scholar
Hubel, D.H. & Wiesel, T.N. (1974). Uniformity of monkey striate cortex: a parallel relationship between field size, scatter, and magnification factor. Journal of Comparative Neurology 158, 295–306.CrossRefGoogle ScholarPubMed
Huerta, M.F. & Harting, J.K. (1984). The mammalian superior colliculus: studies of its morphology and connections. In Comparative Neurology of the Optic Tectum, ed. Vanegas, H., pp. 687–773. New York: Plenum Press.CrossRefGoogle Scholar
Kaneko, C.R.S., Evinger, C. & Fuchs, A.F. (1981). Role of cat pontine burst neurons in generation of saccadic eye movements. Journal of Neurophysiology 46, 387–408.CrossRefGoogle ScholarPubMed
Kawamura, K. & Hashikawa, T. (1978). Cell bodies of origin of reticular projections from the superior colliculus in the cat: An experimental study with the use of horseradish peroxidase as tracer. Journal of Comparative Neurology 182, 1–16.CrossRefGoogle Scholar
Keller, E.L. (1974). Participation of medial pontinereticular formation in eye-movement generation in monkey. Journal of Neurophysiology 37, 316–332.CrossRefGoogle ScholarPubMed
King, W.M. & Fuchs, A. (1979). Reticular control of vertical saccadic eye movements by mesencephalic burst neurons. Journal of Neurophysiology 42, 861–876.CrossRefGoogle ScholarPubMed
Lane, R.H., Allman, J.M., Kaas, J.H. & Miezin, F.M. (1973). The visuotopic organization of the superior colliculus of the owl monkey (Aotus trivirgatus) and the bush baby (Galago senegalensis). Brain Research 60, 335–349.CrossRefGoogle ScholarPubMed
Langer, T., Kaneko, C.R.S., Scudder, C.A. & Fuchs, A.F. (1986). Afferents to the abducens nucleus in the monkey and cat. Journal of Comparative Neurology 245, 379–400.CrossRefGoogle Scholar
Lee, C., Rohrer, W.H. & Sparks, D.L. (1988). Population coding of saccadic eye movements by neurons in the superior colliculus. Nature 332, 357–360.CrossRefGoogle ScholarPubMed
Luschei, E.S. & Fuchs, A.F. (1972). Activity of brain-stem neurons during eye movements of alert monkeys. Journal of Neurophysiology 35, 445–461.CrossRefGoogle ScholarPubMed
Maeda, M., Shibazaki, T. & Yoshida, K. (1979). Labyrinthine and visual inputs to superior colliculus neurons. Progress in Brain Research 50, 735–743.CrossRefGoogle ScholarPubMed
McIlwain, J.T. (1975). Visual receptive fields and their images in superior colliculus of the cat. Journal of Neurophysiology 38, 219–230.CrossRefGoogle ScholarPubMed
McIlwain, J.T. (1976). Large receptive fields and spatial transformations in the visual system. International Review of Physiology 10, 223–248.Google Scholar
McIlwain, J.T. (1982). Lateral spread of neural excitation during microstimulation in intermediate gray layer of cat's superior colliculus. Journal of Neurophysiology 47, 167–178.CrossRefGoogle ScholarPubMed
McIlwain, J.T. (1986). Effects of eye position on saccades evoked electrically from superior colliculus of alert cats. Journal of Neurophysiology 55, 97–112.CrossRefGoogle ScholarPubMed
McIlwaln, J.T. & Buser, P. (1968). Receptive fields of single cells in the cat's superior colliculus. Experimental Brain Research 5, 314–325.Google Scholar
Meredith, M.A. & Stein, B.E. (1986). Visual, auditory, and somatosensory convergence on cells in superior colliculus results in multisensory integration. Journal of Neurophysiology 56, 640–662.CrossRefGoogle ScholarPubMed
Middlebrooks, J.C. & Knudsen, E.I. (1984). A neural code for auditory space in the cat's superior colliculus. Journal of Neuroscience 4, 2621–2635.CrossRefGoogle ScholarPubMed
Mize, R.R. (1988). Immunocytochemical localization of gamma-aminobutyric acid (GABA) in the cat superior colliculus. Journal of Comparative Neurology 276, 169–188.CrossRefGoogle ScholarPubMed
Mohler, C.W. & Wurtz, R.H. (1976). Organization of monkey superior colliculus: Intermediate layer cells discharging before eye movements. Journal of Neurophysiology 39, 722–744.CrossRefGoogle ScholarPubMed
Mohler, C.W. & Wurtz, R.H. (1977). Role of Striate cortex and superior colliculus in visual guidance of saccadic eye movements in monkeys. Journal of Neurophysiology 40, 74–94.CrossRefGoogle ScholarPubMed
Moschovakis, A.K. & Karabelas, A.B. (1982). Tectotectal interactions in the cat. Society for Neuroscience Abstracts 8, 293.Google Scholar
Moschovakis, A.K. & Karabelas, A.B. (1985). Observations on the somatodendritic morphology and axonal trajectory of intracellularly HRP-labeled efferent neurons located in the deeper layers of the Superior colliculus of the cat. Journal of Comparative Neurology 239, 276–308.CrossRefGoogle ScholarPubMed
Moschovakis, A.K., Karabelas, A.B. & Highstein, S.M. (1988). Structure-function relationships in the primate superior colliculus, II: Morphological identity of presaccadic neurons. Journal of Neurophysiology 60, 263–302.CrossRefGoogle ScholarPubMed
Munoz, D.P. & Guitton, D. (1985). Tectospinal neurons in the cat have discharges coding gaze position error. Brain Research 341, 184–188.CrossRefGoogle ScholarPubMed
Munoz, D.P. & Guitton, D. (1987). Tecto-reticulo-spinal neurons have discharges coding the velocity profiles of eye and head orienting movements. Society for Neuroscience Abstracts 13, 393.Google Scholar
Munoz, D.P. & Guitton, D. (1989). Fixation and orientation control by the tecto-reticulo-spinal system in the cat whose head is unrestrained. Revue Neurologique 145, 567–579.Google ScholarPubMed
Munoz, D.P., Guitton, D. & Pelisson, D. (1989). Gaze control in the head-free cat, II: Spatiotemporal variations in the discharge of superior colliculus output neurons. Society for Neuroscience Abstracts 15, 807.Google Scholar
Ottes, F.B. (1985). Saccade eye movement responses to visual target/nontarget stimuli in man and monkey. Ph.D. Thesis, Catholic University of Nijmegen.Google Scholar
Ottes, F.B., Van, Gisbergen J.A.M. & Eggermont, J.J. (1986). Visuomotor fields of the superior colliculus: a quantitative model. Vision Research 26, 857–874.CrossRefGoogle ScholarPubMed
Peck, C.K. (1984). Saccade-related neurons in cat superior colliculus: pandirectional movement cells with postsaccadic responses. Journal of Neurophysiology 52 1154–1168.CrossRefGoogle ScholarPubMed
Peck, C.K., Schlag-Rey, M. & Schlag, J. (1980). Visuo-oculomotor properties of cells in the superior colliculus of the alert cat. Journal of Comparative Neurology 194, 97–116.CrossRefGoogle ScholarPubMed
Pitts, W. & McCulloch, W.S. (1947). How we know universals: The perception of auditory and visual forms. Bulletin of Mathematical Biophysics 9, 127–147.CrossRefGoogle ScholarPubMed
Raybourn, M.S. & Keller, E.L. (1977). Colliculoreticular organization in primate oculomotor system. Journal of Neurophysiology 40, 861–878.CrossRefGoogle ScholarPubMed
Richmond, B.J., Optican, L.M. & Spitzer, H. (1990). Temporal encoding of two-dimensional patterns by single units in primate primary visual cortex, I: Stimulus-response relations. Journal of Neurophysiology 64, 351–369.CrossRefGoogle ScholarPubMed
Robinson, D.A. (1972). Eye movements evoked by collicular stimulation in the alert monkey. Vision Research 12, 1795–1808.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. 337–374. Oxford: Pergamon Press.Google Scholar
Robinson, D.L. & Jarvis, C.D. (1974). Superior colliculus neurons studied during head and eye movements of the behaving monkey. Journal of Neurophysiology 37, 533–540.CrossRefGoogle ScholarPubMed
Robinson, D.L. & McClurkin, J.W. (1989). The visual superior colliculus and pulvinar. In The Neurobiology of Saccadic Eye Movements. Reviews in Oculomotor Research, Vol. 3, ed. Wutrz, R.H. & Goldberg, M.E., pp. 337–360. Amsterdam: Elsevier.Google Scholar
Rohrer, W., White, J. & Sparks, D. (1987). Saccade-related burst cells in the superior colliculus: relationship of activity with saccadic velocity. Society for Neuroscience Abstracts 13, 1092.Google Scholar
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, 75–86.CrossRefGoogle ScholarPubMed
Schiller, P.H. & Koerner, F. (1971). Discharge characteristics of single units in superior colliculus of the alert rhesus monkey. Journal of Neurophysiology 34, 920–936.CrossRefGoogle ScholarPubMed
Schiller, P.H. & Stryker, M. (1972). Single-unit recording and stimulation in superior colliculus of the alert rhesus monkey. Journal of Neurophysiology 35, 915–924.CrossRefGoogle ScholarPubMed
Schiller, P.H., True, S.D. & Conway, J.L. (1979). Paired stimulation of the frontal eye fields and the superior colliculus of the rhesus monkey. Brain Research 179, 162–164.CrossRefGoogle ScholarPubMed
Schiller, P.H., True, S.D. & Conway, J.L. (1980). Deficits in eye movements following frontal eye-field and superior colliculus ablations. Journal of Neurophysiology 44, 1175–1189.CrossRefGoogle ScholarPubMed
Sparks, D.L. (1986). Translation of sensory signals into commands for control of saccadic eye movements: Role of primate superior colliculus. Physiological Reviews 66, 118–171.CrossRefGoogle ScholarPubMed
Sparks, D.L. & Hartwich-Young, R. (1989). The deep layers of the superior colliculus. In The Neurobiology of Saccadic Eye Movements. Reviews in Oculomotor Research, Vol. 3, ed. Wurtz, R.H. & Goldberg, M.E., pp. 213–255.Amsterdam: Elsevier.Google Scholar
Sparks, D.L. & Mays, L.E. (1990). Signal transformations required for the generation of saccadic eye movements. Annual Review of Neuroscience 13, 309–336.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, 21–34.CrossRefGoogle ScholarPubMed
Stanton, G.B. & Greene, R.W. (1981). Brain-stem afferents to the periabducens reticular formations (PARF) in the cat–an HRP study. Experimental Brain Research 44, 419–426.CrossRefGoogle Scholar
Stein, B.E. & Arigbede, M.O. (1972). Unimodal and multimodal response properties of neurons in the cat's superior colliculus. Experimental Neurology 36, 179–196.CrossRefGoogle ScholarPubMed
Stein, B.E., Magalhāes-Castro, B. & Kruger, L. (1976). Relationship between visual and tactile representations in cat superior colliculus. Journal of Neurophysiology 39, 401–419.CrossRefGoogle ScholarPubMed
Sterling, P. & Wicklgren, B.G. (1969). Visual receptive fields in the superior colliculus of the cat. Journal of Neurophysiology 32, 1–15.CrossRefGoogle ScholarPubMed
Straschill, M. & Hoffmann, K.-P. (1970). Activity of movement sensitive neurones of the cat's tectum opticum during spontaneous eye movements. Experimental Brain Research 11, 318–326.CrossRefGoogle ScholarPubMed
Straschill, M. & Taghavy, A. (1967). Neuronale Reaktionen im Tectum Opticum der Katze auf bewegete und stationäre Lichtreize. Experimental Brain Research 3, 353–367.CrossRefGoogle Scholar
Stryker, M.P. & Schiller, P.H. (1975). Eye and head movements evoked by electrical stimulation of monkey superior colliculus. Experimental Brain Research 23, 103–112.CrossRefGoogle ScholarPubMed
Tweed, D. & Vilis, T. (1985). A two-dimensional model for saccade generation. Biological Cybernetics 52, 219–227.CrossRefGoogle ScholarPubMed
Tweed, D. & Vilis, T. (1987). Implications of rotational kinematics for the oculomotor system in three dimensions. Journal of Neurophysiology 58, 832–849.CrossRefGoogle ScholarPubMed
Tweed, D. & Vilis, T. (1990). The superior colliculus and spatiotemporal translation in the saccadic system. Neural Networks 3, 75–86.CrossRefGoogle Scholar
Updyke, B.V. (1974). Characteristics of unit responses in superior colliculus of Cebus monkey. Journal of Neurophysiology 37, 896–909.CrossRefGoogle ScholarPubMed
Van, Essen D.C., Newsome, W.T. & Maunsell, J.H.R. (1984). The visual-field representation in striate cortex of the macaque monkey: asymmetries, anisotropies, and individual variability. Vision Research 24, 429–448.Google Scholar
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. 69–101. Amsterdam: Elsevier.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, 417–442.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, 541–555.Google Scholar
Van, Opstal A.J. & Van, Gisbergen J.A.M. (1989 a). A model for collicular efferent mechanisms underlying the generation of electrically evoked saccades. Brain, Behavior, and Evolution 33, 90–94.Google Scholar
Van, Opstal A.J. & Van, Gisbergen J.A.M. (1989 b). Analysis of variability in amplitude and direction of saccades. Vision Research 29, 1183–1196.Google Scholar
Van, Opstal A.J. & Van, Gisbergen J.A.M. (1989 c). A nonlinear model for collicular spatial interactions underlying the metrical properties of electrically elicited saccades. Biological Cybernetics 60, 171–183.Google Scholar
Van, Opstal A.J., Van, Gissbergen J.A.M. & Smit, A.C. (1990). Comparison of saccades evoked by visual stimulation and collicular electrical stimulation in the alert monkey. Experimental Brain Research 79, 299–312.Google Scholar
Waitzman, D.M., Ma, T.P., Optican, L.M. & Wutrz, R.H. (1988). Superior colliculus neurons provide the saccadic motor error signal. Experimental Brain Research 73, 649–652.Google Scholar
Westheimer, G. (1957). Kinematics of the eye. Journal of the Optical Society of America 47, 967–974.CrossRefGoogle ScholarPubMed
Wurtz, R.H. & Goldberg, M.E. (1972 a). Activity of superior colliculus in behaving monkey, III: Cells discharging before eye movements. Journal of Neurophysiology 35, 575–586.CrossRefGoogle Scholar
Wurtz, R.H. & Goldberg, M.E. (1972 b). Activity of superior colliculus in behaving monkey, IV: Effects of lesions on eye movements. Journal of Neurophysiology 35, 587–596.CrossRefGoogle ScholarPubMed