Beyond the point of no return: effects of visual distractors on saccade amplitude and velocity.

Visual transients, such as a bright flash, reduce the proportion of saccades executed, ∼60-125 ms after flash onset, a phenomenon known as saccadic inhibition (SI). Across three experiments, we apply a similar time-course analysis to the amplitudes and velocities of saccades. Alongside the expected reduction of saccade frequency in the key time period, we report two perturbations of the "main sequence": one before and one after the period of SI. First, saccades launched between 30 and 70 ms, following the flash, were hypometric, with peak speed exceeding that expected for a saccade of similar amplitude. This finding was in contrast to the common idea that saccades have passed a "point of no return," ∼60 ms before launching, escaping interference from distractors. The early hypometric saccades observed were not a consequence of spatial averaging between target and distractor locations, as they were found not only following a localized central flash (experiment 1) but also following a spatially generalized flash (experiment 2). Second, across experiments, saccades launched at 110 ms postflash, toward the end of SI, had normal amplitude but a peak speed higher than expected for that amplitude, suggesting increased collicular excitation at the time of launching. Overall, the results show that saccades that escape inhibition following a visual transient are not necessarily unaffected but instead, can reveal interference in spatial and kinematic measures.

[1]  C. Clifford,et al.  Adaptation to vergent and averted eye gaze. , 2014, Journal of vision.

[2]  Eyal M. Reingold,et al.  Saccadic Inhibition in Voluntary and Reflexive Saccades , 2002, Journal of Cognitive Neuroscience.

[3]  Ralf Engbert,et al.  Toward a model of microsaccade generation: the case of microsaccadic inhibition. , 2008, Journal of vision.

[4]  J. V. Gisbergen,et al.  Collicular ensemble coding of saccades based on vector summation , 1987, Neuroscience.

[5]  A. Bompas,et al.  Saccadic Inhibition Reveals the Timing of Automatic and Voluntary Signals in the Human Brain , 2011, The Journal of Neuroscience.

[6]  I. Hooge,et al.  The timing of sequences of saccades in visual search , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[7]  Eyal M. Reingold,et al.  SACCADIC INHIBITION IN COMPLEX VISUAL TASKS , 1999 .

[8]  Kitty Z. Xu,et al.  Inhibition of voluntary saccadic eye movement commands by abrupt visual onsets. , 2009, Journal of neurophysiology.

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

[10]  R H Wurtz,et al.  Activity of neurons in monkey superior colliculus during interrupted saccades. , 1996, Journal of neurophysiology.

[11]  J. Henderson,et al.  CRISP: a computational model of fixation durations in scene viewing. , 2010, Psychological review.

[12]  D P Munoz,et al.  Role of Primate Superior Colliculus in Preparation and Execution of Anti-Saccades and Pro-Saccades , 1999, The Journal of Neuroscience.

[13]  J. Fuller,et al.  Head movement propensity , 2004, Experimental Brain Research.

[14]  R. McIntosh,et al.  Saccadic inhibition can cause the remote distractor effect, but the remote distractor effect may not be a useful concept. , 2014, Journal of vision.

[15]  Antje Nuthmann,et al.  Mechanisms of saccadic decision making while encoding naturalistic scenes. , 2015, Journal of vision.

[16]  E. Reingold,et al.  Saccadic Inhibition and Gaze Contingent Research Paradigms , 2000 .

[17]  E. Freedman Coordination of the eyes and head during visual orienting , 2008, Experimental Brain Research.

[18]  A. V. van Opstal,et al.  Dynamic ensemble coding of saccades in the monkey superior colliculus. , 2006, Journal of neurophysiology.

[19]  R. Wurtz,et al.  Saccade-related activity in monkey superior colliculus. I. Characteristics of burst and buildup cells. , 1995, Journal of neurophysiology.

[20]  Iain D Gilchrist,et al.  A population coding account for systematic variation in saccadic dead time. , 2007, Journal of neurophysiology.

[21]  H. Collewijn,et al.  Binocular co‐ordination of human vertical saccadic eye movements. , 1988, The Journal of physiology.

[22]  A. Fuchs,et al.  Activity of omnipause neurons in alert cats during saccadic eye movements and visual stimuli. , 1982, Journal of neurophysiology.

[23]  Eyal M Reingold,et al.  Saccadic inhibition in reading. , 2004, Journal of experimental psychology. Human perception and performance.

[24]  D. Sparks The brainstem control of saccadic eye movements , 2002, Nature Reviews Neuroscience.

[25]  K. Shapiro,et al.  The contingent negative variation (CNV) event-related potential (ERP) predicts the attentional blink , 2008 .

[26]  D. Munoz,et al.  Lateral interactions in the superior colliculus, not an extended fixation zone, can account for the remote distractor effect , 1999, Behavioral and Brain Sciences.

[27]  Antimo Buonocore,et al.  Modulation of saccadic inhibition by distractor size and location , 2012, Vision Research.

[28]  F. Ottes,et al.  Visuomotor fields of the superior colliculus: A quantitative model , 1986, Vision Research.

[29]  E. Keller,et al.  Activity of visuomotor burst neurons in the superior colliculus accompanying express saccades. , 1996, Journal of neurophysiology.

[30]  C. J. Erkelens,et al.  Control of fixation duration in a simple search task , 1996, Perception & psychophysics.

[31]  D. P. Hanes,et al.  Controlled Movement Processing: Superior Colliculus Activity Associated with Countermanded Saccades , 2003, The Journal of Neuroscience.

[32]  Laurence R. Harris,et al.  Small Saccades to Double-Stepped Targets Moving in Two Dimensions , 1984 .

[33]  N. J. Gandhi,et al.  Spatial distribution and discharge characteristics of superior colliculus neurons antidromically activated from the omnipause region in monkey. , 1997, Journal of neurophysiology.

[34]  E. Reingold,et al.  Chapter 17 – Using the Saccadic Inhibition Paradigm to Investigate Saccadic Control in Reading , 2003 .

[35]  G. Rizzolatti,et al.  Neurons with complex visual properties in the superior colliculus of the macaque monkey , 2004, Experimental Brain Research.

[36]  D. Munoz,et al.  Neuronal Activity in Monkey Superior Colliculus Related to the Initiation of Saccadic Eye Movements , 1997, The Journal of Neuroscience.

[37]  L. Stark,et al.  The main sequence, a tool for studying human eye movements , 1975 .

[38]  L E Mays,et al.  Signal transformations required for the generation of saccadic eye movements. , 1990, Annual review of neuroscience.

[39]  Ralf Engbert,et al.  Microsaccades uncover the orientation of covert attention , 2003, Vision Research.

[40]  Alain Guillaume,et al.  Saccadic inhibition is accompanied by large and complex amplitude modulations when induced by visual backward masking. , 2012, Journal of vision.

[41]  Donald Morrill SACCADES , 2010, Fourth Genre: Explorations in Nonfiction.

[42]  Miguel P Eckstein,et al.  Saccadic and perceptual performance in visual search tasks. I. Contrast detection and discrimination. , 2003, Journal of the Optical Society of America. A, Optics, image science, and vision.

[43]  N. J. Gandhi,et al.  Two-dimensional saccade-related population activity in superior colliculus in monkey. , 1998, Journal of neurophysiology.

[44]  A. John van Opstal,et al.  Linear ensemble-coding in midbrain superior colliculus specifies the saccade kinematics , 2008, Biological Cybernetics.

[45]  Colin W G Clifford,et al.  Gaze constancy in upright and inverted faces. , 2015, Journal of vision.

[46]  Antimo Buonocore,et al.  Saccadic inhibition underlies the remote distractor effect , 2008, Experimental Brain Research.

[47]  B. Fischer,et al.  Dead zone for express saccades , 2004, Experimental Brain Research.

[48]  James J. Clark,et al.  Microsaccades as an overt measure of covert attention shifts , 2002, Vision Research.

[49]  Ziad M. Hafed,et al.  On the Dissociation between Microsaccade Rate and Direction after Peripheral Cues: Microsaccadic Inhibition Revisited , 2013, The Journal of Neuroscience.

[50]  Eugene McSorley,et al.  The remote distractor effect in saccade programming: channel interactions and lateral inhibition , 2005, Vision Research.

[51]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[52]  R. McIntosh,et al.  Attention modulates saccadic inhibition magnitude , 2013, Quarterly journal of experimental psychology.

[53]  Y. Benjamini,et al.  THE CONTROL OF THE FALSE DISCOVERY RATE IN MULTIPLE TESTING UNDER DEPENDENCY , 2001 .

[54]  Erik D. Reichle,et al.  Toward a model of eye movement control in reading. , 1998, Psychological review.

[55]  E. Keller,et al.  Use of interrupted saccade paradigm to study spatial and temporal dynamics of saccadic burst cells in superior colliculus in monkey. , 1994, Journal of neurophysiology.

[56]  R. Klein,et al.  A Model of Saccade Initiation Based on the Competitive Integration of Exogenous and Endogenous Signals in the Superior Colliculus , 2001, Journal of Cognitive Neuroscience.