Hostname: page-component-78c5997874-m6dg7 Total loading time: 0 Render date: 2024-11-19T07:19:03.424Z Has data issue: false hasContentIssue false

Short latency ocular-following responses in man

Published online by Cambridge University Press:  02 June 2009

R.S. Gellman
Affiliation:
Department of Clinical Neurosciences, University of Calgary School of Medicine, Alberta, Canada
J.R. Carl
Affiliation:
Laboratory of Sensorimotor Research, National Eye Institute, National Institutes of Health, Bethesda
F.A. Miles
Affiliation:
Laboratory of Sensorimotor Research, National Eye Institute, National Institutes of Health, Bethesda

Abstract

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.

Type
Research Article
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

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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Barnes, G.R. & Crombie, J.W. (1985). The interaction of conflicting retinal motion stimuli in oculomotor control. Experimental Brain Research 59, 548558.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Breitmeyer, B.G. (1984). Visual Masking: An Integrative Approach. Oxford: Clarendon Press.Google Scholar
Brodal, P. (1978). The corticopontine projection in the rhesus monkey. Origins and principles of organization. Brain 101, 251283.CrossRefGoogle ScholarPubMed
Brodal, P. (1979). The pontocerebellar projection in the rhesus monkey: an experimental study with retrograde axonal transport of horseradish peroxidase. Neuroscience 4, 193208.CrossRefGoogle ScholarPubMed
Burr, D.C., Holt, J., Johnstone, J.R. & Ross, J. (1982). Selective depression of motion sensitivity during saccades. Journal of Physiology (London) 333, 115.CrossRefGoogle ScholarPubMed
Burr, D.C. & Ross, J. (1982). Contrast sensitivity at high velocities. Vision Research 22, 479484.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Carl, J.R. & Gellman, R.S. (1987). Human smooth pursuit: stimulusdependent responses. Journal of Neurophysiology 57, 14461463.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Collewijn, H., Van Der Mark, F. & Jansen, T.C. (1975). Precise recordings of human eye movements. Vision Research 15, 447450.CrossRefGoogle ScholarPubMed
Derrington, A.M. (1984). Spatial-frequency selectivity of remote pattern masking. Vision Research 24, 19651968.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.Google ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
Hood, J.D. (1975). Observations upon the role of the peripheral retina in the execution of eye movements. Journal d'Otorhinolaryngolgie 37, 6573.Google ScholarPubMed
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.CrossRefGoogle Scholar
Kapoula, Z.A., Robinson, D.A. & Hain, T.C. (1986). Motion of the eye immediately after a saccade. Experimental Brain Research 61, 386394.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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).Google Scholar
Keller, E.L. & Khan, N.S. (1986). Smooth-pursuit initiation in the presence of a textured background in monkey. Vision Research 26, 943955.CrossRefGoogle ScholarPubMed
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.Google ScholarPubMed
Kowler, E. & Steinman, R.M. (1981). The effect of expectations on slow oculomotor control, III: Guessing unpredictable target displacements. Vision Research 21, 191203.CrossRefGoogle ScholarPubMed
Kruger, J. (1977). The shift-effect in the lateral geniculate body of the rhesus monkey. Experimental Brain Research 29, 387392.Google ScholarPubMed
Kruger, J., Fischer, B. & Barth, R. (1975). The shift-effect in retinal ganglion cells of the rhesus monkey. Experimental Brain Research 23, 443446.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Maunsell, J.H.R. & Newsome, W.T. (1987). Visual processing in monkey extrastriate cortex. Annual Review of Neuroscience 10, 363401.CrossRefGoogle ScholarPubMed
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.Google Scholar
McIlwain, J.T. (1964). Receptive fields of optic tract axons and lateral geniculate cells: peripheral extent and barbiturate sensitivity. Journal of Neurophysiology 27, 11541173.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.Google Scholar
Noda, H. & Suzuki, D.A. (1979). Processing of eye-movement signals in the flocculus of the monkey. Journal of Physiology (London) 294, 349364.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Optican, L.M. & Miles, F.A. (1985). Visually induced adaptive changes in primate saccadic oculomotor control signals. Journal of Neurophysiology 54, 940958.CrossRefGoogle ScholarPubMed
Optican, L.M. & Robinson, D.A. (1980). Cerebellar-dependent adaptive control of primate saccadic system. Journal of Neurophysiology 44, 10581076.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Reichardt, W. (1987). Evaluation of optical motion information by movement detectors. Journal of Comparative Physiology 161, 533547.CrossRefGoogle ScholarPubMed
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.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
Schor, C.M. & Narayan, V. (1981). The influence of field size upon the spatial-frequency response of optokinetic nystagmus. Vision Research 21, 985994.CrossRefGoogle ScholarPubMed
Schwarz, U., Busettini, C. & Miles, F.A. (1989). Ocular responses to linear motion are inversely proportional to viewing distance. Science 245, 13941396.CrossRefGoogle ScholarPubMed
Shioiri, S. & Cavanagh, P. (1989). Saccadic suppression of low-level motion. Vision Research 29, 915928.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Takemori, S. & Cohen, B. (1974). Loss of visual suppression of vestibular nystagmus after flocculus lesions. Brain Research 72, 213224.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Ter Braak, J.W.G. (1957). “Ambivalent” optokinetic stimulation. Folia Psychiatrica, Neurologia et Neurochirurgica Neerlandica 60, 131135.Google ScholarPubMed
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
Tolhurst, D.J. & Movshon, J.A. (1975). Spatial and temporal contrast sensitivity of striate cortical neurones. Nature (London) 257, 674675.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Volkmann, F.C. (1986). Human visual suppression. Vision Research 26, 14011416.CrossRefGoogle ScholarPubMed
Volkmann, F.C., Riggs, L.A., White, K.D. & Moore, R.K. (1978). Contrast sensitivity during saccadic eye movements. Vision Research 18, 11931199.CrossRefGoogle ScholarPubMed
Waespe, W. & Cohen, B. (1983). Flocculectomy and unit activity in the vestibular nuclei during visual-vestibular interactions. Experimental Brain Research 51, 2335.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Weber, R.B. & Daroff, R.B. (1971). The metrics of horizontal saccadic eye movements in normal humans. Vision Research 11, 921928.CrossRefGoogle ScholarPubMed
Weber, R.B. & Daroff, R.B. (1972). Corrective movements following refixation saccades: type and control system analysis. Vision Research 12, 467475.CrossRefGoogle ScholarPubMed
Yamada, J. & Noda, H. (1987). Afferent and efferent connections of the oculomotor cerebellar vermis in the macaque monkey. Journal of Comparative Neurology 265, 224241.CrossRefGoogle ScholarPubMed
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.Google ScholarPubMed
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.CrossRefGoogle ScholarPubMed