Perception during double-step saccades

How the visual system achieves perceptual stability across saccadic eye movements is a long-standing question in neuroscience. It has been proposed that an efference copy informs vision about upcoming saccades, and this might lead to shifting spatial coordinates and suppressing image motion. Here we ask whether these two aspects of visual stability are interdependent or may be dissociated under special conditions. We study a memory-guided double-step saccade task, where two saccades are executed in quick succession. Previous studies have led to the hypothesis that in this paradigm the two saccades are planned in parallel, with a single efference copy signal generated at the start of the double-step sequence, i.e. before the first saccade. In line with this hypothesis, we find that visual stability is impaired during the second saccade, which is consistent with (accurate) efference copy information being unavailable during the second saccade. However, we find that saccadic suppression is normal during the second saccade. Thus, the second saccade of a double-step sequence instantiates a dissociation between visual stability and saccadic suppression: stability is impaired even though suppression is strong.

[1]  D. Burr,et al.  Transient spatiotopic integration across saccadic eye movements mediates visual stability. , 2013, Journal of neurophysiology.

[2]  Frank Bremmer,et al.  Spatiotemporal profile of peri-saccadic contrast sensitivity. , 2011, Journal of vision.

[3]  Eric Castet,et al.  Motion perception of saccade-induced retinal translation , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[4]  K. Hoffmann,et al.  Neural Dynamics of Saccadic Suppression , 2009, Journal of Neuroscience.

[5]  D. Burr,et al.  Selective depression of motion sensitivity during saccades. , 1982, The Journal of physiology.

[6]  Daniel Guitton,et al.  Two distinct types of remapping in primate cortical area V4 , 2016, Nature Communications.

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

[8]  F. C. Volkmann Human visual suppression , 1986, Vision Research.

[9]  Maria Concetta Morrone,et al.  Visual mislocalization during saccade sequences , 2014, Experimental Brain Research.

[10]  C. Bruce,et al.  Primate frontal eye fields. III. Maintenance of a spatially accurate saccade signal. , 1990, Journal of neurophysiology.

[11]  Alexander C. Schütz,et al.  Visual sensitivity for luminance and chromatic stimuli during the execution of smooth pursuit and saccadic eye movements , 2017, Vision Research.

[12]  W. Becker,et al.  An analysis of the saccadic system by means of double step stimuli , 1979, Vision Research.

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

[14]  Bart Krekelberg,et al.  Postsaccadic visual references generate presaccadic compression of space , 2000, Nature.

[15]  J R Duhamel,et al.  The updating of the representation of visual space in parietal cortex by intended eye movements. , 1992, Science.

[16]  L. M. M.-T. Theory of Probability , 1929, Nature.

[17]  Guillaume S. Masson,et al.  Dynamics of Visual Motion Processing: Neuronal, Behavioral, and Computational Approaches , 2014 .

[18]  S. B. Stevenson,et al.  Dependence of visual suppression on the amplitudes of saccades and blinks , 1986, Vision Research.

[19]  Kae Nakamura,et al.  Updating of the visual representation in monkey striate and extrastriate cortex during saccades , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[20]  Robert H Wurtz,et al.  Saccadic Corollary Discharge Underlies Stable Visual Perception , 2016, The Journal of Neuroscience.

[21]  Nao Ninomiya,et al.  The 10th anniversary of journal of visualization , 2007, J. Vis..

[22]  Guillaume S. Masson,et al.  Motion perception during saccadic eye movements , 2000, Nature Neuroscience.

[23]  Jeffrey N. Rouder,et al.  Bayesian t tests for accepting and rejecting the null hypothesis , 2009, Psychonomic bulletin & review.

[24]  R. Wurtz,et al.  A Pathway in Primate Brain for Internal Monitoring of Movements , 2002, Science.

[25]  Maria Concetta Morrone,et al.  Spatiotopic coding and remapping in humans , 2011, Philosophical Transactions of the Royal Society B: Biological Sciences.

[26]  M. Goldberg,et al.  Spatial processing in the monkey frontal eye field. I. Predictive visual responses. , 1997, Journal of neurophysiology.

[27]  M. Rolfs,et al.  Remapping Attention Pointers: Linking Physiology and Behavior , 2016, Trends in Cognitive Sciences.

[28]  E. Castet,et al.  ‘Saccadic suppression’ – no need for an active extra-retinal mechanism , 2001, Trends in Neurosciences.

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

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

[31]  Robert H. Wurtz,et al.  Influence of the thalamus on spatial visual processing in frontal cortex , 2006, Nature.

[32]  Alfonso Caramazza,et al.  Continuous perception of motion and shape across saccadic eye movements. , 2010, Journal of vision.

[33]  G. Westheimer Eye movement responses to a horizontally moving visual stimulus. , 1954, A.M.A. archives of ophthalmology.

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

[35]  Carolina M. Zingale,et al.  Planning sequences of saccades , 1987, Vision Research.

[36]  Robert M. McPeek,et al.  What neural pathways mediate express saccades? , 1993, Behavioral and Brain Sciences.

[37]  A. Levy-Schoen,et al.  On oculomotor programming and perception. , 1974, Brain research.

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

[39]  I. Rock,et al.  Stroboscopic movement based on change of phenomenal rather than retinal location. , 1962, The American journal of psychology.

[40]  P. Cavanagh,et al.  Predictive remapping of attention across eye movements , 2011, Nature Neuroscience.

[41]  Patrick Cavanagh,et al.  Spatiotopic apparent motion reveals local variations in space constancy. , 2011, Journal of vision.

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

[43]  G. Rees,et al.  Saccades Differentially Modulate Human LGN and V1 Responses in the Presence and Absence of Visual Stimulation , 2005, Current Biology.

[44]  David C. Burr,et al.  Compression of visual space before saccades , 1997, Nature.

[45]  Kerry Hourigan,et al.  Wake transition of a rolling sphere , 2011, J. Vis..

[46]  C. Ploner,et al.  Human thalamus contributes to perceptual stability across eye movements , 2009, Proceedings of the National Academy of Sciences.

[47]  David W. Royal,et al.  Correlates of motor planning and postsaccadic fixation in the macaque monkey lateral geniculate nucleus , 2005, Experimental Brain Research.