Chromatic contrast sensitivity during optokinetic nystagmus, visually enhanced vestibulo-ocular reflex, and smooth pursuit eye movements.

Recently we showed that sensitivity for chromatic- and high-spatial frequency luminance stimuli is enhanced during smooth-pursuit eye movements (SPEMs). Here we investigated whether this enhancement is a general property of slow eye movements. Besides SPEM there are two other classes of eye movements that operate in a similar range of eye velocities: the optokinetic nystagmus (OKN) is a reflexive pattern of alternating fast and slow eye movements elicited by wide-field visual motion and the vestibulo-ocular reflex (VOR) stabilizes the gaze during head movements. In a natural environment all three classes of eye movements act synergistically to allow clear central vision during self- and object motion. To test whether the same improvement of chromatic sensitivity occurs during all of these eye movements, we measured human detection performance of chromatic and luminance line stimuli during OKN and contrast sensitivity during VOR and SPEM at comparable velocities. For comparison, performance in the same tasks was tested during fixation. During the slow phase of OKN we found a similar enhancement of chromatic detection rate like that during SPEM, whereas no enhancement was observable during VOR. This result indicates similarities between slow-phase OKN and SPEM, which are distinct from VOR.

[1]  M. Landy,et al.  The effect of viewpoint on perceived visual roughness. , 2007, Journal of vision.

[2]  T. Uemura,et al.  Compensatory eye movement and gaze fixation upon passive head- and body rotation and active head rotation , 2004, Archives of oto-rhino-laryngology.

[3]  Arthur L. Benton,et al.  Reaction time to square-wave gratings as a function of spatial frequency, complexity and contrast , 1975, Brain Research.

[4]  Dominic W. Hughes,et al.  Eye-Tracking Patterns in Schizophrenia , 1973, Science.

[5]  Harold E Bedell,et al.  Signals of eye-muscle proprioception modulate perceived motion smear. , 2008, Journal of vision.

[6]  Johannes M. Zanker,et al.  Smooth-pursuit eye movements elicited by first-order and second-order motion , 1997, Experimental Brain Research.

[7]  Rebekka Lencer,et al.  Eye movements and psychiatric disease , 2004, Current opinion in neurology.

[8]  R. Leigh,et al.  The neurology of eye movements , 1984 .

[9]  R. L. Nó,et al.  VESTIBULO-OCULAR REFLEX ARC , 1933 .

[10]  Harold E. Bedell,et al.  Attenuation of perceived motion smear during the vestibulo-ocular reflex , 2005, Vision Research.

[11]  D. Burr,et al.  Selective suppression of the magnocellular visual pathway during saccadic eye movements , 1994, Nature.

[12]  U. Ilg,et al.  Initiation of smooth-pursuit eye movements to first-order and second-order motion stimuli , 2000, Experimental Brain Research.

[13]  Eli Brenner,et al.  Smooth eye movements and spatial localisation , 2001, Vision Research.

[14]  G. Barnes,et al.  Vision during angular oscillation: the dynamic interaction of visual and vestibular mechanisms. , 1978, Aviation, space, and environmental medicine.

[15]  W. P. Huebner,et al.  Performance of the human vestibuloocular reflex during locomotion. , 1989, Journal of neurophysiology.

[16]  T. Freeman,et al.  Extra-Retinal Vision: Firing at Will , 2007, Current Biology.

[17]  F. Campbell,et al.  Saccadic omission: Why we do not see a grey-out during a saccadic eye movement , 1978, Vision Research.

[18]  V. Dietz,et al.  Fast head tilt has only a minor effect on quick compensatory reactions during the regulation of stance and gait , 2004, Experimental Brain Research.

[19]  R. Krauzlis The Control of Voluntary Eye Movements: New Perspectives , 2005, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[20]  G. L. Walls The evolutionary history of eye movements , 1962 .

[21]  R. Carpenter,et al.  Movements of the Eyes , 1978 .

[22]  M. B. Bender,et al.  Ocular stabilization during oscillatory head movements. , 1968, Archives of neurology.

[23]  Dennis M. Levi,et al.  Reaction time as a measure of suprathreshold grating detection , 1978, Vision Research.

[24]  Stephen G Lisberger,et al.  Gain control in human smooth-pursuit eye movements. , 2002, Journal of neurophysiology.

[25]  Harold E. Bedell,et al.  Direction and extent of perceived motion smear during pursuit eye movement , 2007, Vision Research.

[26]  Jefferson E. Roy,et al.  Signal processing in the vestibular system during active versus passive head movements. , 2004, Journal of neurophysiology.

[27]  F. Bremmer,et al.  Expansion of visual space during optokinetic afternystagmus (OKAN). , 2008, Journal of neurophysiology.

[28]  Harold E. Bedell,et al.  Asymmetry of perceived motion smear during head and eye movements: Evidence for a dichotomous neural categorization of retinal image motion , 2005, Vision Research.

[29]  T. Sejnowski,et al.  Learning and memory in the vestibulo-ocular reflex. , 1995, Annual review of neuroscience.

[30]  Gert Hauske,et al.  Perceptual latencies to sinusoidal gratings , 1976, Vision Research.

[31]  A. T. Smith,et al.  Motion defined exclusively by second-order characteristics does not evoke optokinetic nystagmus , 1992, Visual Neuroscience.

[32]  S. Lisberger,et al.  The Cerebellum: A Neuronal Learning Machine? , 1996, Science.

[33]  F. Bremmer,et al.  Localization of visual targets during optokinetic eye movements , 2007, Vision Research.

[34]  S. Lisberger The neural basis for motor learning in the vestibulo-ocular reflex in monkeys , 1988, Trends in Neurosciences.

[35]  Seiji Ono,et al.  Extraretinal signals in MSTd neurons related to volitional smooth pursuit. , 2006, Journal of neurophysiology.

[36]  W P Medendorp,et al.  Context compensation in the vestibuloocular reflex during active head rotations. , 2000, Journal of neurophysiology.

[37]  Claes von Hofsten,et al.  Development of gaze tracking of small and large objects , 2002, Experimental Brain Research.

[38]  C. Hofsten An action perspective on motor development , 2004, Trends in Cognitive Sciences.

[39]  Eli Brenner,et al.  Mislocalization of flashes during smooth pursuit hardly depends on the lighting conditions , 2006, Vision Research.

[40]  C. Von Hofsten,et al.  Visual-vestibular interaction in early infancy , 2000, Experimental Brain Research.

[41]  D. Burr,et al.  The effect of optokinetic nystagmus on the perceived position of briefly flashed targets , 2007, Vision Research.

[42]  S. Martinez-Conde,et al.  Fixational eye movements across vertebrates: comparative dynamics, physiology, and perception. , 2008, Journal of vision.

[43]  U Büttner,et al.  Present concepts of oculomotor organization. , 1988, Reviews of oculomotor research.

[44]  P. Pichot,et al.  Eye-tracking patterns in schizophrenia. An analysis based on the incidence of saccades. , 1981, Archives of general psychiatry.

[45]  P. Holzman,et al.  Optokinetic nystagmus and pursuit eye movements in schizophrenia. , 1981, Archives of general psychiatry.

[46]  Milena Mihaylova,et al.  Peripheral and central delay in processing high spatial frequencies: reaction time and VEP latency studies , 1999, Vision Research.

[47]  Stephen G. Lisberger,et al.  Regulation of the gain of visually guided smooth-pursuit eye movements by frontal cortex , 2001, Nature.

[48]  Karl R. Gegenfurtner,et al.  Contrast sensitivity during the initiation of smooth pursuit eye movements , 2007, Vision Research.

[49]  T Fujishiro,et al.  Studies of the vestibulo-ocular reflex and visual-vestibular interactions during active head movements. , 1980, Acta oto-laryngologica.

[50]  Comparison of smooth pursuit and combined eye-head tracking in human subjects with deficient labyrinthine function , 2004, Experimental Brain Research.

[51]  F. Bremmer,et al.  An fMRI study of optokinetic nystagmus and smooth-pursuit eye movements in humans , 2005, Experimental Brain Research.

[52]  S. Lisberger,et al.  Initial tracking conditions modulate the gain of visuo-motor transmission for smooth pursuit eye movements in monkeys , 1994, Visual Neuroscience.

[53]  Peter Thier,et al.  The neural basis of smooth pursuit eye movements in the rhesus monkey brain , 2008, Brain and Cognition.

[54]  R. Krauzlis Recasting the smooth pursuit eye movement system. , 2004, Journal of neurophysiology.

[55]  R. J. Leigh,et al.  Frequency and velocity of rotational head perturbations during locomotion , 2004, Experimental Brain Research.

[56]  W. Becker,et al.  Gaze Stabilization by Optokinetic Reflex (OKR) and Vestibulo-ocular Reflex (VOR) During Active Head Rotation in Man , 1997, Vision Research.

[57]  Karl R Gegenfurtner,et al.  Temporal contrast sensitivity during smooth pursuit eye movements. , 2007, Journal of vision.

[58]  Harold E Bedell,et al.  Suppression of motion-produced smear during smooth pursuit eye movements , 1996, Current Biology.

[59]  A. Fuchs,et al.  Infant eye movements: Quantification of the vestibulo-ocular reflex and visual-vestibular interactions , 1991, Vision Research.

[60]  U. Ilg Visual-tracking neurons in area MST are activated during anticipatory pursuit eye movements , 2003, Neuroreport.

[61]  Gary D. Paige,et al.  Senescence of human visual-vestibular interactions: smooth pursuit, optokinetic, and vestibular control of eye movements with aging , 2004, Experimental Brain Research.

[62]  Laurence R. Harris,et al.  Interactions between first- and second-order motion revealed by optokinetic nystagmus , 1999, Experimental Brain Research.

[63]  R D Yee,et al.  Effects of an optokinetic background on pursuit eye movements. , 1983, Investigative ophthalmology & visual science.

[64]  U. Ilg Slow eye movements , 1997, Progress in Neurobiology.

[65]  Jefferson E. Roy,et al.  A neural correlate for vestibulo-ocular reflex suppression during voluntary eye–head gaze shifts , 1998, Nature Neuroscience.

[66]  M. Morrone,et al.  Extraretinal Control of Saccadic Suppression , 2000, The Journal of Neuroscience.

[67]  Dirk Kerzel,et al.  Improved visual sensitivity during smooth pursuit eye movements , 2010 .

[68]  P. Thier,et al.  Posterior Parietal Cortex Neurons Encode Target Motion in World-Centered Coordinates , 2004, Neuron.

[69]  Frank Bremmer,et al.  Optokinetic and pursuit system: A case report , 1993, Behavioural Brain Research.

[70]  G D Paige,et al.  Vestibuloocular reflex and its interactions with visual following mechanisms in the squirrel monkey. I. Response characteristics in normal animals. , 1983, Journal of neurophysiology.

[71]  P. Lennie,et al.  Chromatic mechanisms in lateral geniculate nucleus of macaque. , 1984, The Journal of physiology.

[72]  M J Hawken,et al.  Pursuit eye movements to second-order motion targets. , 2001, Journal of the Optical Society of America. A, Optics, image science, and vision.

[73]  K Nakayama,et al.  Dependence of impaired eye tracking on deficient velocity discrimination in schizophrenia. , 1999, Archives of general psychiatry.

[74]  Jefferson E. Roy,et al.  Vestibuloocular reflex signal modulation during voluntary and passive head movements. , 2002, Journal of neurophysiology.

[75]  H. Levitt Transformed up-down methods in psychoacoustics. , 1971, The Journal of the Acoustical Society of America.

[76]  M. B. Bender,et al.  Ocular Stabilization During Oscillatory Head Movements: Vestibular System Dysfunction and the Relation Between Head and Eye Velocities , 1968 .

[77]  F A Wichmann,et al.  Ning for Helpful Comments and Suggestions. This Paper Benefited Con- Siderably from Conscientious Peer Review, and We Thank Our Reviewers the Psychometric Function: I. Fitting, Sampling, and Goodness of Fit , 2001 .

[78]  R M Steinman,et al.  Compensatory eye movements during active and passive head movements: fast adaptation to changes in visual magnification. , 1983, The Journal of physiology.

[79]  P. Thier,et al.  Visual tracking neurons in primate area MST are activated by smooth-pursuit eye movements of an "imaginary" target. , 2003, Journal of neurophysiology.