Spatiotopic updating facilitates perception immediately after saccades

As the neural representation of visual information is initially coded in retinotopic coordinates, eye movements (saccades) pose a major problem for visual stability. If no visual information were maintained across saccades, retinotopic representations would have to be rebuilt after each saccade. It is currently strongly debated what kind of information (if any at all) is accumulated across saccades and when this information becomes available after a saccade. Here, we use a motion illusion to examine the accumulation of visual information across saccades. In this illusion, an annulus with a random texture slowly rotates and is then replaced with a second texture (motion transient). With increasing rotation durations, observers consistently perceive the transient as large rotational jumps in the direction opposite to rotation direction (backward jumps). We first show that accumulated motion information is updated spatiotopically across saccades. Then, we show that this accumulated information is readily available after a saccade, immediately biasing postsaccadic perception. The current findings suggest that presaccadic information is used to facilitate postsaccadic perception and are in support of a forward model of transsaccadic perception, aiming at anticipating the consequences of eye movements and operating within the narrow perisaccadic time window.

[1]  E. Zohary,et al.  Rapid Formation of Spatiotopic Representations As Revealed by Inhibition of Return , 2010, The Journal of Neuroscience.

[2]  James A. Mazer,et al.  Perisaccadic Updating of Visual Representations and Attentional States: Linking Behavior and Neurophysiology , 2016, Front. Syst. Neurosci..

[3]  Ronald A. Rensink,et al.  Change blindness: past, present, and future , 2005, Trends in Cognitive Sciences.

[4]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[5]  Kenji Kawano,et al.  Eye position effects on the remapped memory trace of visual motion in cortical area MST , 2016, Scientific Reports.

[6]  Wilsaan M Joiner,et al.  Quantifying the spatial extent of the corollary discharge benefit to transsaccadic visual perception. , 2016, Journal of neurophysiology.

[7]  C. Cierpka,et al.  Particle imaging techniques for volumetric three-component (3D3C) velocity measurements in microfluidics , 2011, Journal of Visualization.

[8]  Marc A Sommer,et al.  The frontal eye field as a prediction map. , 2008, Progress in brain research.

[9]  Patrick Cavanagh,et al.  Default perception of high-speed motion , 2013, Proceedings of the National Academy of Sciences.

[10]  A. Mizuno,et al.  A change of the leading player in flow Visualization technique , 2006, J. Vis..

[11]  T. Moore,et al.  Saccades and shifting receptive fields: anticipating consequences or selecting targets? , 2014, Trends in Cognitive Sciences.

[12]  L. Marshall,et al.  Evidence for Optimal Integration of Visual Feature Representations across Saccades , 2015, The Journal of Neuroscience.

[13]  M. Goldberg,et al.  The time course of perisaccadic receptive field shifts in the lateral intraparietal area of the monkey. , 2003, Journal of neurophysiology.

[14]  R. M. Siegel,et al.  Maps of Visual Space in Human Occipital Cortex Are Retinotopic, Not Spatiotopic , 2008, The Journal of Neuroscience.

[15]  David E. Irwin,et al.  The role of the saccade target object in the perception of a visually stable world , 2000, Perception & psychophysics.

[16]  Keith Rayner,et al.  Transsaccadic processing: stability, integration, and the potential role of remapping , 2015, Attention, perception & psychophysics.

[17]  P. Wenderoth,et al.  Retinotopic encoding of the direction aftereffect , 2008, Vision Research.

[18]  Matthew D. Hilchey,et al.  Oculomotor inhibition of return: How soon is it “recoded” into spatiotopic coordinates? , 2012, Attention, Perception, & Psychophysics.

[19]  Eckart Zimmermann,et al.  Spatial Position Information Accumulates Steadily over Time , 2013, The Journal of Neuroscience.

[20]  Bruce Bridgeman,et al.  Failure to detect displacement of the visual world during saccadic eye movements , 1975, Vision Research.

[21]  Maria Concetta Morrone,et al.  Spatiotopic neural representations develop slowly across saccades , 2013, Current Biology.

[22]  Jan Theeuwes,et al.  Visual attention and stability , 2011, Philosophical Transactions of the Royal Society B: Biological Sciences.

[23]  Jan Theeuwes,et al.  Dissociating oculomotor contributions to spatial and feature-based selection. , 2013, Journal of neurophysiology.

[24]  D G Pelli,et al.  The VideoToolbox software for visual psychophysics: transforming numbers into movies. , 1997, Spatial vision.

[25]  David Melcher,et al.  Spatiotopic temporal integration of visual motion across saccadic eye movements , 2003, Nature Neuroscience.

[26]  R. Wurtz,et al.  Visual Perception and Corollary Discharge , 2008, Perception.

[27]  R. Baayen,et al.  Mixed-effects modeling with crossed random effects for subjects and items , 2008 .

[28]  Nicholas A. Steinmetz,et al.  Visual Space is Compressed in Prefrontal Cortex Before Eye Movements , 2014, Nature.

[29]  Marc A Sommer,et al.  Frontal Eye Field Neurons Assess Visual Stability Across Saccades , 2012, The Journal of Neuroscience.

[30]  B. Bridgeman,et al.  Postsaccadic target blanking prevents saccadic suppression of image displacement , 1996, Vision Research.

[31]  Julie D. Golomb,et al.  Robustness of the retinotopic attentional trace after eye movements. , 2010, Journal of vision.

[32]  Patrick Cavanagh,et al.  Allocation of attention across saccades , 2012 .

[33]  P. Cavanagh,et al.  Saccadic suppression of low-level motion , 1989, Vision Research.

[34]  U. Ilg,et al.  Visual Stability and the Motion Aftereffect: A Psychophysical Study Revealing Spatial Updating , 2011, PloS one.

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

[36]  Jan Theeuwes,et al.  Feature based attention and visual stability , 2012 .

[37]  Paul M Bays,et al.  Spatial remapping of the visual world across saccades , 2007, Neuroreport.

[38]  D. Burr,et al.  Spatiotopic selectivity of BOLD responses to visual motion in human area MT , 2007, Nature Neuroscience.

[39]  Bart Krekelberg,et al.  Summation of Visual Motion across Eye Movements Reflects a Nonspatial Decision Mechanism , 2010, The Journal of Neuroscience.

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

[41]  Mark Wexler,et al.  Orthogonal steps relieve saccadic suppression. , 2014, Journal of vision.

[42]  Christopher B. Currie,et al.  Visual stability across saccades while viewing complex pictures. , 1995, Journal of experimental psychology. Human perception and performance.

[43]  P. Cavanagh,et al.  Visual stability based on remapping of attention pointers , 2010, Trends in Cognitive Sciences.

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

[45]  Daniel M. Wolpert,et al.  Forward Models for Physiological Motor Control , 1996, Neural Networks.

[46]  Patrick Cavanagh,et al.  The reference frame of the motion aftereffect is retinotopic. , 2009, Journal of vision.

[47]  Peter J Bex,et al.  Integrating Retinotopic Features in Spatiotopic Coordinates , 2014, The Journal of Neuroscience.

[48]  Wilsaan M. Joiner,et al.  Neuronal mechanisms for visual stability: progress and problems , 2011, Philosophical Transactions of the Royal Society B: Biological Sciences.

[49]  Jan Theeuwes,et al.  A reinvestigation of the reference frame of the tilt-adaptation aftereffect , 2013, Scientific Reports.

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

[51]  Stefan Treue,et al.  An Attention-Sensitive Memory Trace in Macaque MT Following Saccadic Eye Movements , 2016, PLoS biology.

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

[53]  B. Webb Neural mechanisms for prediction: do insects have forward models? , 2004, Trends in Neurosciences.

[54]  John P. John,et al.  Assessing Neurocognition via Gamified Experimental Logic: A Novel Approach to Simultaneous Acquisition of Multiple ERPs , 2016, Front. Neurosci..

[55]  David C. Burr,et al.  Spatiotopic Coding of BOLD Signal in Human Visual Cortex Depends on Spatial Attention , 2011, PloS one.

[56]  Eero P. Simoncelli,et al.  Near-optimal integration of orientation information across saccades. , 2015, Journal of vision.

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

[58]  Alexander C. Schütz,et al.  Trans-saccadic integration of peripheral and foveal feature information is close to optimal. , 2015, Journal of vision.

[59]  Johan Wagemans,et al.  Transsaccadic identification of highly similar artificial shapes. , 2009, Journal of vision.

[60]  Kenji Kawano,et al.  Neurons in cortical area MST remap the memory trace of visual motion across saccadic eye movements , 2014, Proceedings of the National Academy of Sciences.

[61]  T. Jaeger,et al.  Categorical Data Analysis: Away from ANOVAs (transformation or not) and towards Logit Mixed Models. , 2008, Journal of memory and language.

[62]  Frans A. J. Verstraten,et al.  Perceptual manifestations of fast neural plasticity: Motion priming, rapid motion aftereffect and perceptual sensitization , 2005, Vision Research.

[63]  C. Colby,et al.  Trans-saccadic perception , 2008, Trends in Cognitive Sciences.