Oculomotor Adaptation Elicited By Intra-Saccadic Visual Stimulation: Time-Course of Efficient Visual Target Perturbation

Perception of our visual environment strongly depends on saccadic eye movements, which in turn are calibrated by saccadic adaptation mechanisms elicited by systematic movement errors. Current models of saccadic adaptation assume that visual error signals are acquired only after saccade completion, because the high speed of saccade execution disturbs visual processing (saccadic “suppression” and “mislocalization”). Complementing a previous study from our group, here we report that visual information presented during saccades can drive adaptation mechanisms and we further determine the critical time window of such error processing. In 15 healthy volunteers, shortening adaptation of reactive saccades toward a ±8° visual target was induced by flashing the target for 2 ms less eccentrically than its initial location either near saccade peak velocity (“PV” condition) or peak deceleration (“PD”) or saccade termination (“END”). Results showed that, as compared to the “CONTROL” condition (target flashed at its initial location upon saccade termination), saccade amplitude decreased all throughout the “PD” and “END” conditions, reaching significant levels in the second adaptation and post-adaptation blocks. The results of nine other subjects tested in a saccade lengthening adaptation paradigm with the target flashing near peak deceleration (“PD” and “CONTROL” conditions) revealed no significant change of gain, confirming that saccade shortening adaptation is easier to elicit. Also, together with this last result, the stable gain observed in the “CONTROL” conditions of both experiments suggests that mislocalization of the target flash is not responsible for the saccade shortening adaptation demonstrated in the first group. Altogether, these findings reveal that the visual “suppression” and “mislocalization” phenomena related to saccade execution do not prevent brief visual information delivered “in-flight” from being processed to elicit oculomotor adaptation.

[1]  P Dassonville,et al.  Oculomotor localization relies on a damped representation of saccadic eye displacement in human and nonhuman primates , 1992, Visual Neuroscience.

[2]  B. Bridgeman,et al.  Relation between cognitive and motor-oriented systems of visual position perception. , 1979, Journal of experimental psychology. Human perception and performance.

[3]  T Anstis,et al.  Saccadic plasticity: parametric adaptive control by retinal feedback. , 1981, Journal of experimental psychology. Human perception and performance.

[4]  Romeo Chua,et al.  The hand’s automatic pilot can update visual information while the eye is in motion , 2009, Experimental Brain Research.

[5]  Kaoru Yoshida,et al.  Memory of Learning Facilitates Saccadic Adaptation in the Monkey , 2004, The Journal of Neuroscience.

[6]  J. Ditterich,et al.  Intrasaccadic target steps during the deceleration of primary saccades affect the latency of corrective saccades , 1999, Experimental Brain Research.

[7]  Anna Ma-Wyatt,et al.  Seeing and ballistic pointing at perisaccadic targets. , 2005, Journal of vision.

[8]  P. Thier,et al.  Reduced saccadic resilience and impaired saccadic adaptation due to cerebellar disease , 2007, The European journal of neuroscience.

[9]  Christopher T. Noto,et al.  Characteristics of simian adaptation fields produced by behavioral changes in saccade size and direction. , 1999, Journal of neurophysiology.

[10]  Heiner Deubel,et al.  Rapid gain adaptation affects the dynamics of saccadic eye movements in humans , 1995, Vision Research.

[11]  Mark Shelhamer,et al.  Sensorimotor adaptation error signals are derived from realistic predictions of movement outcomes. , 2011, Journal of neurophysiology.

[12]  A. ALEXASDER,et al.  ACCURACY OF SPATIAL LOCALIZATIONS NEAR THE TIME OF SACCADIC EYE MOVEMENTS , 2002 .

[13]  Mark Shelhamer,et al.  Using prediction errors to drive saccade adaptation: the implicit double-step task , 2012, Experimental Brain Research.

[14]  Denis Pélisson,et al.  Eye position specificity of saccadic adaptation. , 2004, Investigative ophthalmology & visual science.

[15]  A. Fuchs,et al.  The characteristics and neuronal substrate of saccadic eye movement plasticity , 2004, Progress in Neurobiology.

[16]  E. Matin Saccadic suppression: a review and an analysis. , 1974, Psychological bulletin.

[17]  David Burr,et al.  Suppression of the magnocellular pathway during saccades , 1996, Behavioural Brain Research.

[18]  Christopher J Bockisch,et al.  Different motor systems use similar damped extraretinal eye position information , 1999, Vision Research.

[19]  L. Optican,et al.  Slow saccades in spinocerebellar degeneration. , 1976, Archives of neurology.

[20]  M. Goodale,et al.  Visual pathways to perception and action. , 1993, Progress in brain research.

[21]  Reza Shadmehr,et al.  Changes in Control of Saccades during Gain Adaptation , 2008, The Journal of Neuroscience.

[22]  Bruce Bridgeman,et al.  An unbiased measure of the contributions of chroma and luminance to saccadic suppression of displacement , 2002, Experimental Brain Research.

[23]  Eileen Kowler,et al.  The control of saccadic adaptation: implications for the scanning of natural visual scenes , 2000, Vision Research.

[24]  H. Honda The time courses of visual mislocalization and of extraretinal eye position signals at the time of vertical saccades , 1991, Vision Research.

[25]  Peter Thier,et al.  The role of the cerebellum in saccadic adaptation as a window into neural mechanisms of motor learning , 2011, The European journal of neuroscience.

[26]  H. Honda Modification of saccade-contingent visual mislocalization by the presence of a visual frame of reference , 1999, Vision Research.

[27]  M. Goodale,et al.  An evolving view of duplex vision: separate but interacting cortical pathways for perception and action , 2004, Current Opinion in Neurobiology.

[28]  Scott E. Bevans,et al.  Effect of visual error size on saccade adaptation in monkey. , 2003, Journal of neurophysiology.

[29]  D. Pélisson,et al.  Sensorimotor adaptation of saccadic eye movements , 2010, Neuroscience & Biobehavioral Reviews.

[30]  C. Prablanc,et al.  Large adjustments in visually guided reaching do not depend on vision of the hand or perception of target displacement , 1986, Nature.

[31]  Yuki Kaku,et al.  Saccade adaptation as a model of learning in voluntary movements , 2010, Experimental Brain Research.

[32]  David C. Burr,et al.  Separate visual representations for perception and action revealed by saccadic eye movements , 2001, Current Biology.

[33]  D. Pélisson,et al.  Sensory Processing of Motor Inaccuracy Depends on Previously Performed Movement and on Subsequent Motor Corrections: A Study of the Saccadic System , 2011, PloS one.

[34]  Josh Wallman,et al.  End-Point Variability Is Not Noise in Saccade Adaptation , 2013, PloS one.

[35]  Reza Shadmehr,et al.  Some Perspectives on Saccade Adaptation , 2009, Annals of the New York Academy of Sciences.

[36]  H Honda,et al.  The extraretinal signal from the pursuit-eye-movement system: Its role in the perceptual and the egocentric localization systems , 1990, Perception & psychophysics.

[37]  D. Pélisson,et al.  On-line modification of saccadic eye movements by retinal signals , 2003, Neuroreport.

[38]  D. Pélisson,et al.  Effect of saccadic adaptation on sequences of saccades , 2012 .

[39]  Bruce Bridgeman,et al.  A theory of visual stability across saccadic eye movements , 1994, Behavioral and Brain Sciences.

[40]  P. E. Hallett,et al.  Saccadic eye movements towards stimuli triggered by prior saccades , 1976, Vision Research.

[41]  Markus Lappe,et al.  Differences in intersaccadic adaptation transfer between inward and outward adaptation. , 2011, Journal of neurophysiology.

[42]  Ned Jenkinson,et al.  The Role of the Posterior Cerebellum in Saccadic Adaptation: A Transcranial Direct Current Stimulation Study , 2015, The Journal of Neuroscience.

[43]  Markus Lappe,et al.  Mislocalization of stationary and flashed bars after saccadic inward and outward adaptation of reactive saccades. , 2012, Journal of neurophysiology.

[44]  M. Banks,et al.  How does saccade adaptation affect visual perception? , 2008, Journal of vision.

[45]  Norio Izumi,et al.  Broadening the visualization frontier , 2007, J. Vis..

[46]  Paul Dassonville,et al.  The use of egocentric and exocentric location cues in saccadic programming , 1995, Vision Research.

[47]  M. Ibbotson,et al.  Visual perception and saccadic eye movements , 2011, Current Opinion in Neurobiology.

[48]  A. Fuchs,et al.  Characteristics of saccadic gain adaptation in rhesus macaques. , 1997, Journal of neurophysiology.

[49]  Denis Pélisson,et al.  Transcranial magnetic stimulation and motor plasticity in human lateral cerebellum: Dual effect on saccadic adaptation , 2012, Human brain mapping.

[50]  Denis Pélisson,et al.  Behavioral evidence of separate adaptation mechanisms controlling saccade amplitude lengthening and shortening. , 2009, Journal of neurophysiology.

[51]  L. Matin,et al.  Visual Perception of Direction for Stimuli Flashed During Voluntary Saccadic Eye Movements , 1965, Science.

[52]  Denis Pélisson,et al.  Brain Processing of Visual Information during Fast Eye Movements Maintains Motor Performance , 2013, PloS one.

[53]  T. Anderson,et al.  Suppression of displacement in severely slowed saccades , 2000, Vision Research.

[54]  L. Matin,et al.  Visual perception of direction when voluntary saccades occur. I. Relation of visual direction of a fixation target extinguished before a saccade to a flash presented during the saccade , 1969 .

[55]  P. E. Hallett,et al.  Saccadic eye movements to flashed targets , 1976, Vision Research.

[56]  C. Prablanc,et al.  Error-correcting mechanisms in large saccades , 1978, Vision Research.

[57]  Peter Thier,et al.  Cerebellar-dependent motor learning is based on pruning a Purkinje cell population response , 2008, Proceedings of the National Academy of Sciences.

[58]  H. Honda Perceptual localization of visual stimuli flashed during saccades , 1989, Perception & psychophysics.

[59]  M. Goodale,et al.  Chapter 28 Visual pathways to perception and action , 1993 .

[60]  J. M. Miller,et al.  Egocentric localization of a perisaccadic flash by manual pointing , 1996, Vision Research.

[61]  B. L. Zuber,et al.  Saccadic suppression: elevation of visual threshold associated with saccadic eye movements. , 1966, Experimental neurology.

[62]  M. Lappe,et al.  Motor signals in visual localization. , 2010, Journal of vision.

[63]  Junle Wang,et al.  Study of depth bias of observers in free viewing of still stereoscopic synthetic stimuli , 2012 .

[64]  S. C. Mclaughlin Parametric adjustment in saccadic eye movements , 1967 .

[65]  Thérèse Collins,et al.  The relative importance of retinal error and prediction in saccadic adaptation. , 2012, Journal of neurophysiology.