Visual attention is available at a task-relevant location rapidly after a saccade

Maintaining attention at a task-relevant spatial location while making eye-movements necessitates a rapid, saccade-synchronized shift of attentional modulation from the neuronal population representing the task-relevant location before the saccade to the one representing it after the saccade. Currently, the precise time at which spatial attention becomes fully allocated to the task-relevant location after the saccade remains unclear. Using a fine-grained temporal analysis of human peri-saccadic detection performance in an attention task, we show that spatial attention is fully available at the task-relevant location within 30 milliseconds after the saccade. Subjects tracked the attentional target veridically throughout our task: i.e. they almost never responded to non-target stimuli. Spatial attention and saccadic processing therefore co-ordinate well to ensure that relevant locations are attentionally enhanced soon after the beginning of each eye fixation. DOI: http://dx.doi.org/10.7554/eLife.18009.001

[1]  Julie D. Golomb,et al.  Attention doesn’t slide: spatiotopic updating after eye movements instantiates a new, discrete attentional locus , 2011, Attention, perception & psychophysics.

[2]  M. Sommer,et al.  Shifting attention to neurons , 2010, Trends in Cognitive Sciences.

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

[4]  Julie D. Golomb,et al.  Attentional Facilitation throughout Human Visual Cortex Lingers in Retinotopic Coordinates after Eye Movements , 2010, The Journal of Neuroscience.

[5]  Eric Castet,et al.  Spatiotemporal dynamics of visual attention during saccade preparation: Independence and coupling between attention and movement planning. , 2007, Journal of vision.

[6]  H. Deubel,et al.  Saccade target selection and object recognition: Evidence for a common attentional mechanism , 1996, Vision Research.

[7]  Devan V Mehrotra,et al.  A Cautionary Note on Exact Unconditional Inference for a Difference between Two Independent Binomial Proportions , 2003, Biometrics.

[8]  C. Pierrot-Deseilligny,et al.  Cortical control of saccades , 1998, Experimental Brain Research.

[9]  Mingsha Zhang,et al.  Parietal Cortical Neuronal Activity Is Selective for Express Saccades , 2013, The Journal of Neuroscience.

[10]  P. Bex,et al.  Peri-Saccadic Natural Vision , 2013, The Journal of Neuroscience.

[11]  B. Dosher,et al.  External noise distinguishes attention mechanisms , 1998, Vision Research.

[12]  Patrick Cavanagh,et al.  Attentional trade-offs maintain the tracking of moving objects across saccades. , 2015, Journal of neurophysiology.

[13]  Patrick Cavanagh,et al.  Allocation of attention across saccades. , 2013, Journal of neurophysiology.

[14]  Julie D. Golomb,et al.  The Native Coordinate System of Spatial Attention Is Retinotopic , 2008, The Journal of Neuroscience.

[15]  Robert W. Kentridge,et al.  Eye movement research : mechanisms, processes and applications , 1995 .

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

[17]  J. Hoffman,et al.  The role of visual attention in saccadic eye movements , 1995, Perception & psychophysics.

[18]  Denis Pélisson,et al.  Adaptation of reactive and voluntary saccades: different patterns of adaptation revealed in the antisaccade task , 2009, The Journal of physiology.

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

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

[21]  H. Spekreijse,et al.  Correlates of transsaccadic integration in the primary visual cortex of the monkey. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

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

[23]  D. Melcher The missing link for attention pointers: comment on Cavanagh et al. , 2010, Trends in Cognitive Sciences.

[24]  L. Brown,et al.  Interval Estimation for a Binomial Proportion , 2001 .

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

[26]  Marcus Nyström,et al.  Post-saccadic oscillations in eye movement data recorded with pupil-based eye trackers reflect motion of the pupil inside the iris , 2013, Vision Research.

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

[28]  L. Stark,et al.  Dynamic overshoot in saccadic eye movements is caused by neurological control signal reversals , 1975, Experimental Neurology.

[29]  B. Krekelberg Saccadic suppression , 2010, Current Biology.

[30]  J. Movshon,et al.  The Timing of Response Onset and Offset in Macaque Visual Neurons , 2002, The Journal of Neuroscience.

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

[32]  Christoph J. Ploner,et al.  Effects of Cortical Lesions on Saccadic , 2002 .

[33]  Mark Shelhamer,et al.  Saccades exhibit abrupt transition between reactive and predictive; predictive saccade sequences have long-term correlations. , 2003, Journal of neurophysiology.

[34]  C. Kennard,et al.  Predictive eye saccades are different from visually triggered saccades , 1987, Vision Research.

[35]  H. Deubel Is saccadic adaptation context-specific? , 1995 .

[36]  Gerald Westheimer,et al.  Grouping of contextual elements that affect vernier thresholds. , 2007, Journal of vision.

[37]  C. Pierrot-Deseilligny,et al.  Effects of cortical lesions on saccadic: eye movements in humans. , 2002, Annals of the New York Academy of Sciences.

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

[39]  Matthew F. Peterson,et al.  Statistical decision theory to relate neurons to behavior in the study of covert visual attention , 2009, Vision Research.

[40]  Roger L. Berger,et al.  Power comparison of exact unconditional tests for comparing two binomial proportions , 1994 .

[41]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[42]  M. Goldberg,et al.  A Rapid and Precise On-Response in Posterior Parietal Cortex , 2004, The Journal of Neuroscience.

[43]  R. Wurtz Neuronal mechanisms of visual stability , 2008, Vision Research.

[44]  Lester C. Loschky,et al.  Perception onset time during fixations in free viewing , 2002, Behavior research methods, instruments, & computers : a journal of the Psychonomic Society, Inc.