Spatiotemporal Distortions of Visual Perception at the Time of Saccades

Both space and time are grossly distorted during saccades. Here we show that the two distortions are strongly linked, and that both could be a consequence of the transient remapping mechanisms that affect visual neurons perisaccadically. We measured perisaccadic spatial and temporal distortions simultaneously by asking subjects to report both the perceived spatial location of a perisaccadic vertical bar (relative to a remembered ruler), and its perceived timing (relative to two sounds straddling the bar). During fixation and well before or after saccades, bars were localized veridically in space and in time. In different epochs of the perisaccadic interval, temporal perception was subject to different biases. At about the time of the saccadic onset, bars were temporally mislocalized 50–100 ms later than their actual presentation and spatially mislocalized toward the saccadic target. Importantly, the magnitude of the temporal distortions co-varied with the spatial localization bias and the two phenomena had similar dynamics. Within a brief period about 50 ms before saccadic onset, stimuli were perceived with shorter latencies than at other delays relative to saccadic onset, suggesting that the perceived passage of time transiently inverted its direction. Based on this result we could predict the inversion of perceived temporal order for two briefly flashed visual stimuli. We developed a model that simulates the perisaccadic transient change of neuronal receptive fields predicting well the reported temporal distortions. The key aspects of the model are the dynamics of the “remapped” activity and the use of decoder operators that are optimal during fixation, but are not updated perisaccadically.

[1]  C L Colby,et al.  Visual, saccade-related, and cognitive activation of single neurons in monkey extrastriate area V3A. , 2000, Journal of neurophysiology.

[2]  G. Sperling,et al.  Attention gating in short-term visual memory. , 1986, Psychological review.

[3]  S. Kitazawa,et al.  Reversal of subjective temporal order due to sensory and motor integrations , 2006 .

[4]  David Burr,et al.  Time Perception: Space–Time in the Brain , 2006, Current Biology.

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

[6]  John E. Schlerf,et al.  Dedicated and intrinsic models of time perception , 2008, Trends in Cognitive Sciences.

[7]  M Concetta Morrone,et al.  Neural mechanisms for timing visual events are spatially selective in real-world coordinates , 2007, Nature Neuroscience.

[8]  M Concetta Morrone,et al.  Saccadic eye movements cause compression of time as well as space , 2005, Nature Neuroscience.

[9]  D. Burr Temporal summation of moving images by the human visual system , 1981, Proceedings of the Royal Society of London. Series B. Biological Sciences.

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

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

[12]  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.

[13]  John C. Rothwell,et al.  Illusory perceptions of space and time preserve cross-saccadic perceptual continuity , 2001, Nature.

[14]  H. D. L. Dzn Research into the dynamic nature of the human fovea-cortex systems with intermittent and modulated light. I. Attenuation characteristics with white and colored light. , 1958 .

[15]  W. B. Pillsbury Lectures or the Elementary Psychology of Feeling and Attention , 1909 .

[16]  Catalin V. Buhusi,et al.  What makes us tick? Functional and neural mechanisms of interval timing , 2005, Nature Reviews Neuroscience.

[17]  C. Genovese,et al.  Spatial Updating in Human Parietal Cortex , 2003, Neuron.

[18]  M. Kenward,et al.  An Introduction to the Bootstrap , 2007 .

[19]  R. Nichols,et al.  Prediction of the first year college performance of high aptitude students. , 1963, Psychological monographs.

[20]  M. Concetta Morrone,et al.  Apparent Position of Visual Targets during Real and Simulated Saccadic Eye Movements , 1997, The Journal of Neuroscience.

[21]  Maria Concetta Morrone,et al.  A model for the distortions of space and time perception during saccades , 2009 .

[22]  P. Tse,et al.  Attention and the subjective expansion of time , 2004, Perception & psychophysics.

[23]  Frank Bremmer,et al.  Neural Correlates of Visual Localization and Perisaccadic Mislocalization , 2003, Neuron.

[24]  C. Spence,et al.  Visual Prior Entry , 2001, Psychological science.

[25]  Vincent P. Ferrera,et al.  Visual Remapping by Vector Subtraction: Analysis of Multiplicative Gain Field Models , 2007, Neural Computation.

[26]  A. Watson Probability summation over time , 1979, Vision Research.

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

[28]  C. Genovese,et al.  Remapping in human visual cortex. , 2007, Journal of neurophysiology.

[29]  M M Merzenich,et al.  Temporal information transformed into a spatial code by a neural network with realistic properties , 1995, Science.

[30]  E. J. Tehovnik,et al.  Eye Movements Modulate Visual Receptive Fields of V4 Neurons , 2001, Neuron.

[31]  D. Burr,et al.  Keeping vision stable: rapid updating of spatiotopic receptive fields may cause relativistic-like effects , 2010 .

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

[33]  David C Burr,et al.  Fusion of Visual and Auditory Stimuli during Saccades: A Bayesian Explanation for Perisaccadic Distortions , 2007, The Journal of Neuroscience.

[34]  Robert Sekuler,et al.  Handbook of Sensory Physiology, Vol. 7/4, Visual Psychophysics , 1973 .

[35]  A. Pouget,et al.  Efficient computation and cue integration with noisy population codes , 2001, Nature Neuroscience.

[36]  Richard A. Andersen,et al.  A back-propagation programmed network that simulates response properties of a subset of posterior parietal neurons , 1988, Nature.

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

[38]  M. Treisman Temporal discrimination and the indifference interval. Implications for a model of the "internal clock". , 1963, Psychological monographs.

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

[40]  R. Andersen,et al.  Models of the Posterior Parietal Cortex Which Perform Multimodal Integration and Represent Space in Several Coordinate Frames , 2000, Journal of Cognitive Neuroscience.

[41]  Derek H. Arnold,et al.  Spatially Localized Distortions of Event Time , 2006, Current Biology.

[42]  D. Eagleman Human time perception and its illusions , 2008, Current Opinion in Neurobiology.

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

[44]  Anthony J. Movshon,et al.  Optimal representation of sensory information by neural populations , 2006, Nature Neuroscience.

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

[46]  David C. Burr,et al.  Spatiotopic selectivity for location of events in space and time , 2010 .

[47]  P. Haggard,et al.  Voluntary action and conscious awareness , 2002, Nature Neuroscience.

[48]  Madeleine Schlag-Rey,et al.  Spatial localization precedes temporal determination in visual perception , 2003, Vision Research.

[49]  O. Braddick Visual psychophysics , 1997, Current Biology.

[50]  M. Goldberg,et al.  Saccades, salience and attention: the role of the lateral intraparietal area in visual behavior. , 2006, Progress in brain research.

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

[52]  Jordan Pola,et al.  Models of the mechanism underlying perceived location of a perisaccadic flash , 2004, Vision Research.

[53]  M. Morrone,et al.  Spatio-temporal distortions of visual perception during saccades , 2007 .

[54]  D. Burr,et al.  Changes in visual perception at the time of saccades , 2001, Trends in Neurosciences.

[55]  M. Lappe,et al.  Spatio-temporal contingency of saccade-induced chronostasis , 2007, Experimental Brain Research.