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Short latency ocular-following responses in man

  • R.S. Gellman (a1), J.R. Carl (a2) and F.A. Miles (a2)

The ocular-following responses elicited by brief unexpected movements of the visual scene were studied in human subjects. Response latencies varied with the type of stimulus and decreased systematically with increasing stimulus speed but, unlike those of monkeys, were not solely determined by the temporal frequency generated by sine-wave stimuli. Minimum latencies (70–75 ms) were considerably shorter than those reported for other visually driven eye movements. The magnitude of the responses to sine-wave stimuli changed markedly with stimulus speed and only slightly with spatial frequency over the ranges used. When normalized with respect to spatial frequency, all responses shared the same dependence on temporal frequency (band-pass characteristics with a peak at 16 Hz), indicating that temporal frequency, rather than speed per se, was the limiting factor over the entire range examined. This suggests that the underlying motion detectors respond to the local changes in luminance associated with the motion of the scene. Movements of the scene in the immediate wake of a saccadic eye movement were on average twice as effective as movements 600 ms later: post-saccadic enhancement. Less enhancement was seen in the wake of saccade-like shifts of the scene, which themselves elicited weak ocular following, something not seen in the wake of real saccades. We suggest that there are central mechanisms that, on the one hand, prevent the ocular-following system from tracking the visual disturbances created by saccades but, on the other, promote tracking of any subsequent disturbance and thereby help to suppress post-saccadic drift. Partitioning the visual scene into central and peripheral regions revealed that motion in the periphery can exert a weak modulatory influence on ocular-following responses resulting from motion at the center. We suggest that this may help the moving observer to stabilize his/her eyes on nearby stationary objects.

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Allman J.M., Meizin F. & McGuinness E. (1985). Direction and velocity-specific responses from beyond the classical receptive field in the middle temporal visual area (MT). Perception 14, 105126.
Bahill A.T., Clark M.R. & Stark L. (1975). Glissades–eye movements generated by mismatched components of the saccadic motoneuronal control signal. Mathematical Biosciences 26, 303.
Barnes G.R. & Crombie J.W. (1985). The interaction of conflicting retinal motion stimuli in oculomotor control. Experimental Brain Research 59, 548558.
Bloedel J.R. & Ebner T.J.(1985). Climbing fiber function: regulation of Purkinje cell responsiveness. In Cerebellar Functions, ed. Bloedel J.R., Dichgans J. & Precht W., pp. 247259. Berlin, Heidelberg: Springer-Verlag.
Bloedel J.R., Ebner T.J. & Yu Q.-X. (1983). Increased responsiveness of Purkinje cells associated with climbing-fiber inputs to neighboring neurons. Journal of Neurophysiology 50, 220239.
Breitmeyer B.G. (1984). Visual Masking: An Integrative Approach. Oxford: Clarendon Press.
Brodal P. (1978). The corticopontine projection in the rhesus monkey. Origins and principles of organization. Brain 101, 251283.
Brodal P. (1979). The pontocerebellar projection in the rhesus monkey: an experimental study with retrograde axonal transport of horseradish peroxidase. Neuroscience 4, 193208.
Burr D.C., Holt J., Johnstone J.R. & Ross J. (1982). Selective depression of motion sensitivity during saccades. Journal of Physiology (London) 333, 115.
Burr D.C. & Ross J. (1982). Contrast sensitivity at high velocities. Vision Research 22, 479484.
Büttner U. & Waespe W. (1984). Purkinje cell activity in the primate flocculus during optokinetic stimulation, smooth-pursuit eye movements and VOR-suppression. Experimental Brain Research 55, 97104.
Carl J.R. & Gellman R.S. (1987). Human smooth pursuit: stimulusdependent responses. Journal of Neurophysiology 57, 14461463.
Cohen B., Matsuo V. & Raphan T. (1977). Quantitative analysis of the velocity characteristics of optokinetic nystagmus and optokinetic after-nystagmus. Journal of Physiology (London) 270, 321344.
Collewijn H. & Tamminga E.P. (1984). Human smooth and saccadic eye movements during voluntary pursuit of different target motions on different backgrounds. Journal of Physiology (London) 351, 217250.
Collewijn H., Van Der Mark F. & Jansen T.C. (1975). Precise recordings of human eye movements. Vision Research 15, 447450.
Derrington A.M. (1984). Spatial-frequency selectivity of remote pattern masking. Vision Research 24, 19651968.
Ebner T.J., Yu Q.-X. & Bloedel J.R. (1983). Increase in Purkinje cell gain associated with naturally activated climbing-fiber input. Journal of Neurophysiology 50, 205219.
Foster K.H., Gaska J.P., Nagler M. & Pollen D.A. (1985). Spatial- and temporal-frequency selectivity of neurones in visual cortical areas Vl and V2 of the macaque monkey. Journal of Physiology (London) 365, 331363.
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, 209229.
Glickstein M., May J.G. & Mercier 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, 343359.
Guedry F.E. Jr., Lentz J.M., Jell R.M. & Norman J.W. (1981). Visual-vestibular interactions: the directional component of visual background movement. Aviation, Space and Environmental Medicine 52, 304309.
Harwerth R.S. & Smith E.L. (1985). Rhesus monkey as a model for normal vision of humans. American Journal of Optometry and Physiological Optics 62, 633641.
Hausen K. (1984). The lobula-complex of the fly: structure, function, and significance in visual behaviour. In Photoreception and Vision in Invertebrates, ed. Ali M.A., pp. 523559. New York: Plenum Press.
Hays A.V., Richmond B.J. & Optican L.M. (1982). A UNIX-based multiple process system for real-time data acquisition and control. WESCON Conference Proceedings 2, (1), 110.
Holub R.A. & Morton-Gibson M. (1981). Response of visual cortical neurons of the cat to moving sinusoidal gratings: response contrast functions and spatiotemporal interactions. Journal of Neurophysiology 46, 12441259.
Hood J.D. (1975). Observations upon the role of the peripheral retina in the execution of eye movements. Journal d'Otorhinolaryngolgie 37, 6573.
Ikeda H. & Wright M.J. (1975). Spatial and temporal properties of “sustained” and “transient” neurones in area 17 of the cat's visual cortex. Experimental Brain Research 22, 363383.
Kapoula Z.A., Robinson D.A. & Hain T.C. (1986). Motion of the eye immediately after a saccade. Experimental Brain Research 61, 386394.
Kawano K. & Miles F.A. (1986). Short-latency ocular-following responses of monkey, II: Dependence on a prior saccadic eye movement. Journal of Neurophysiology 56, 13551380.
Kawano K., Watanabe Y., Kaji S. & Yamane S. (1990). Neuronal activity in the posterior parietal cortex and pontine nucleus of alert monkey during ocular-following responses. In Vision, Memory, and the Temporal Lobe, ed. Iwai E., New York: Elsevier (in press).
Keller E.L. & Khan N.S. (1986). Smooth-pursuit initiation in the presence of a textured background in monkey. Vision Research 26, 943955.
Kommerell G., Olivier D. & Theopold H. (1976). Adaptive programming of phasic and tonic components in saccadic eye movements. Investigation in patients with abducens palsy. Investigative Ophthalmology 15, 657660.
Kowler E. & Steinman R.M. (1981). The effect of expectations on slow oculomotor control, III: Guessing unpredictable target displacements. Vision Research 21, 191203.
Kruger J. (1977). The shift-effect in the lateral geniculate body of the rhesus monkey. Experimental Brain Research 29, 387392.
Kruger J., Fischer B. & Barth R. (1975). The shift-effect in retinal ganglion cells of the rhesus monkey. Experimental Brain Research 23, 443446.
Langer T., Fuchs A.F., Scudder C.A. & Chubb M.C. (1985). Afferents to the flocculus of the cerebellum in the rhesus macaque as revealed by retrograde transport of horseradish peroxidase. Journal of Comparative Neurology 235, 125.
Leventhal A.G., Rodieck R.W. & Dreher B. (1981). Retinal ganglion cell classes in cat and Old World monkey: morphology and central projections. Science 213, 11391142.
Levick W.R., Oyster C.W. & Davis D.L. (1965). Evidence that McIlwain's periphery effect is not a stray light artefact. Journal of Neurophysiology 28, 555559.
Lisberger S.G. & Fuchs A.F. (1978). Role of primate flocculus during rapid behavioral modification of vestibuloocular reflex, I: Purkinje cell activity during visually guided horizontal smooth-pursuit eye movements and passive head rotation. Journal of Neurophysiology 41, 733777.
Markert G., Büttner U., Straube A. & Boyle R. (1988). Neoronal activity in the flocculus of the alert monkey during sinusoidal optokinetic stimulation. Experimental Brain Research 70, 134144.
Maunsell J.H.R. & Newsome W.T. (1987). Visual processing in monkey extrastriate cortex. Annual Review of Neuroscience 10, 363401.
May J.G., Keller E.L. & Crandall W.F. (1985). Changes in eye velocity during smooth-pursuit tracking induced by microstimulation in the dorsolateral pontine nucleus of the macaque. Society for Neuroscience Abstracts 11, 79.
McIlwain J.T. (1964). Receptive fields of optic tract axons and lateral geniculate cells: peripheral extent and barbiturate sensitivity. Journal of Neurophysiology 27, 11541173.
Miles F.A., Fuller J.H., Braitman D.J. & Dow B.M. (1980). Long-term adaptive changes in primate vestibuloocular reflex, III: Electrophysiological observations in flocculus of normal monkeys. Journal of Neurophysiology 43, 14371476.
Miles F.A., Kawano K. & Optican L.M. (1986). Short-latency ocular-following responses of monkey, I: Dependence on temporospatial properties of the visual input. Journal of Neurophysiology 56, 13211354.
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, 664686.
Noda H. (1986). Mossy fibers sending retinal-slip, eye, and head velocity signals to the flocculus of the monkey. Journal of Physiology (London) 379, 3960.
Noda H., Asoh R., & Shibagaki M. (1977). Floccular unit activity associated with eye movements and fixation. In Control of Gaze Brain Stem Neurons ed. Baker R. & Berthoz A., pp. 371380. Amsterdam, New York: Elsevier/North-Holland Biomedical Press.
Noda H. & Suzuki D.A. (1979). Processing of eye-movement signals in the flocculus of the monkey. Journal of Physiology (London) 294, 349364.
Noda H. & Warabi T. (1986). Discharges of Purkinje cells in monkey's flocculus during smooth-pursuit eye movements and visual stimulus movements. Experimental Neurology 93, 390403.
Optican L.M. & Miles F.A. (1985). Visually induced adaptive changes in primate saccadic oculomotor control signals. Journal of Neurophysiology 54, 940958.
Optican L.M. & Robinson D.A. (1980). Cerebellar-dependent adaptive control of primate saccadic system. Journal of Neurophysiology 44, 10581076.
Pointer J.S. & Hess R.F. (1989). The contrast-sensitivity gradient across the human visual field: with emphasis on the low spatial-frequency range. Vision Research 29, 11331151.
Reichardt W. (1987). Evaluation of optical motion information by movement detectors. Journal of Comparative Physiology 161, 533547.
Robinson D.A. (1963). A method of measuring eye movement using a scleral search coil in a magnetic field. IEEE Transactions on Bio-Medical Engineering BME-10, 137145.
Ron S. & Robinson D.A. (1973). Eye movements evoked by cerebellar stimulation in the alert monkey. Journal of Neurophysiology 36, 10041022.
Schor C.M. & Narayan V. (1981). The influence of field size upon the spatial-frequency response of optokinetic nystagmus. Vision Research 21, 985994.
Schwarz U., Busettini C. & Miles F.A. (1989). Ocular responses to linear motion are inversely proportional to viewing distance. Science 245, 13941396.
Shioiri S. & Cavanagh P. (1989). Saccadic suppression of low-level motion. Vision Research 29, 915928.
Stone L.S. & Lisberger S.G. (1989). Synergistic action of complex and simple spikes in the monkey flocculus in the control of smooth-pursuit eye movement. Experimental Brain Research (Suppl.) 17, 299312.
Suzuki D.A. & Keller E.L. (1984). Visual signals in the dorsolateral pontine nucleus of the alert monkey: their relationship to smooth-pursuit eye movements. Experimental Brain Research 53, 473478.
Suzuki D.A. & Keller E.L. (1988 a). Role of the posterior vermis of monkey cerebellum in smooth-pursuit eye movement control, I: Eye and head movement-related activity. Journal of Neurophysiology 59, 118.
Suzuki D.A. & Keller E.L. (1988 b). Role of the posterior vermis of monkey cerebellum in smooth-pursuit eye movement control, II: Target velocity-related Purkinje cell activity. Journal of Neurophysiology 59, 1940.
Suzuki D.A., May J.G., Keller E.L. & Yee R.D. (1990). Visualmotor response properties of neurons in dorsolateral pontine nucleus of alert monkey. Journal of Neurophysiology 63, 3759.
Suzuki D.A., Noda H. & Kase M. (1981). Visual and pursuit eye movement-related activity in posterior vermis of the monkey cerebellum. Journal of Neurophysiology 46, 11201139.
Takemori S. & Cohen B. (1974). Loss of visual suppression of vestibular nystagmus after flocculus lesions. Brain Research 72, 213224.
Tanaka K., Hikosaka K., Saito H.A., Yukie M., Fukada Y. & Iwai E. (1986). Analysis of local and wide-field movements in the superior temporal visual areas of the macaque monkey. Journal of Neuroscience 6, 134144.
Ter Braak J.W.G. (1957). “Ambivalent” optokinetic stimulation. Folia Psychiatrica, Neurologia et Neurochirurgica Neerlandica 60, 131135.
Ter Braak J.W.G. (1962). Optokinetic control of eye movements, in particular optokinetic nystagmus. Proceedings 22nd International Congress of Physiological Sciences (Leiden) 1, 502505.
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. Experimental Brain Research 70, 496512.
Tolhurst D.J. & Movshon J.A. (1975). Spatial and temporal contrast sensitivity of striate cortical neurones. Nature (London) 257, 674675.
Tootell R.B.H., Hamilton S.L. & Switkes E. (1988). Functional anatomy of macaque striate cortex, IV: Contrast and magno-parvo streams. Journal of Neuroscience 8, 15941609.
Volkmann F.C. (1986). Human visual suppression. Vision Research 26, 14011416.
Volkmann F.C., Riggs L.A., White K.D. & Moore R.K. (1978). Contrast sensitivity during saccadic eye movements. Vision Research 18, 11931199.
Waespe W. & Cohen B. (1983). Flocculectomy and unit activity in the vestibular nuclei during visual-vestibular interactions. Experimental Brain Research 51, 2335.
Waespe W., Cohen B. & Raphan T. (1983). Role of the flocculus and paraflocculus in optokinetic nystagmus and visual-vestibular interactions: effects of lesions. Experimental Brain Research 50, 933.
Waespe W., Rudinger D. & Wolfensberger M. (1985). Purkinje cell activity in the flocculus of vestibular neurectomized and normal monkeys during optokinetic nystagmus (OKN) and smooth-pursuit eye movements. Experimental Brain Research 60, 243262.
Weber R.B. & Daroff R.B. (1971). The metrics of horizontal saccadic eye movements in normal humans. Vision Research 11, 921928.
Weber R.B. & Daroff R.B. (1972). Corrective movements following refixation saccades: type and control system analysis. Vision Research 12, 467475.
Yamada J. & Noda H. (1987). Afferent and efferent connections of the oculomotor cerebellar vermis in the macaque monkey. Journal of Comparative Neurology 265, 224241.
Yee R.D., Daniels S.A., Jones O.W., Baloh R.W. & Honrubia V. (1983). Effects of an optokinetic background on pursuit eye movements. Investigative Ophthalmology and Visual Science 24, 11151122.
Zee D.S., Yamazaki A., Butler P.H. & Gücer G. (1981). Effects of ablation of flocculus and paraflocculus on eye movements in primate. Journal of Neurophysiology 46, 878899.
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Visual Neuroscience
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