Discriminating between anticipatory and visually triggered saccades: measuring minimal visual saccadic response time using luminance.

We describe a novel behavioral method to accurately discriminate anticipatory (i.e., saccades not generated by visual input) from visually triggered saccades and to identify the minimal visual saccadic reaction time (SRT). This method can be used to calculate a feasible lower bound cutoff for latencies of visually triggered saccades within a certain experimental context or participant group. We apply this method to compute the minimal visual SRT for two different saccade target luminance levels. Three main findings are presented: 1) the minimal visual SRT for all participants was 46 ms shorter for bright targets than for dim targets, 2) the transition from non-visually triggered to visually triggered saccades occurred abruptly, independent of target luminance, and 3) although the absolute minimal visual SRTs varied between participants, the response pattern (response to bright targets being faster than to dim targets) was consistent across participants. These results are consistent with variability in saccadic and neural responses to luminance as has been reported in monkeys. On the basis of these results, we argue that differences in the minimal visual SRT can easily occur when stimuli vary in luminance or other saliency features. Applying an absolute cutoff (i.e., 70-90 ms) that approaches the minimal neuronal conduction delays, which is general practice in many laboratories, may result in the wrongful inclusion of saccades that are not visually triggered. It is suggested to assess the lower SRT bound for visually triggered saccades when piloting an experimental setup and before including saccades based on particular latency criteria. NEW & NOTEWORTHY We successfully developed an anticipation paradigm to discriminate between anticipatory and visually triggered saccades by measuring the minimal visual saccadic response time (SRT). We show that the 70- to 90-ms lower bound cutoff for visually triggered saccades should be applied in a flexible way and that the transitional interval is very short. The paradigm can be employed to investigate the effects of different stimulus features, experimental conditions, and participant groups on the minimal visual SRT in humans.

[1]  B. Ramsden,et al.  Selective impairment of express saccade generation in patients with schizophrenia , 2004, Experimental Brain Research.

[2]  Laurent Itti,et al.  Superior colliculus neurons encode a visual saliency map during free viewing of natural dynamic video , 2017, Nature Communications.

[3]  Petroc Sumner,et al.  Sensory sluggishness dissociates saccadic, manual, and perceptual responses: an S-cone study. , 2008, Journal of vision.

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

[5]  D. Sparks,et al.  The role of the superior colliculus in saccade initiation: a study of express saccades and the gap effect , 2000, Vision Research.

[6]  B. Fischer,et al.  Separate populations of visually guided saccades in humans: reaction times and amplitudes , 2004, Experimental Brain Research.

[7]  A. Opstal,et al.  Stimulus intensity modifies saccadic reaction time and visual response latency in the superior colliculus , 2006, Experimental Brain Research.

[8]  J. V. Gisbergen,et al.  A parametric analysis of human saccades in different experimental paradigms , 1987, Vision Research.

[9]  S. Brandt,et al.  Salience from multiple feature contrast: Evidence from saccade trajectories , 2018, Attention, perception & psychophysics.

[10]  J. Theeuwes,et al.  Programming of endogenous and exogenous saccades: evidence for a competitive integration model. , 2002, Journal of experimental psychology. Human perception and performance.

[11]  Daniel Cavegn.  Bilateral interactions in saccade programming , 1996, Experimental Brain Research.

[12]  W. Becker.  The neurobiology of saccadic eye movements. Metrics. , 1989, Reviews of oculomotor research.

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

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

[15]  R. Carpenter,et al.  Contrast, Probability, and Saccadic Latency Evidence for Independence of Detection and Decision , 2004, Current Biology.

[16]  P. E. Hallett,et al.  The differentiation of visually guided and anticipatory saccades in gap and overlap paradigms , 2004, Experimental Brain Research.

[17]  D. Munoz,et al.  Age-related performance of human subjects on saccadic eye movement tasks , 1998, Experimental Brain Research.

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

[19]  D. Munoz,et al.  Saccadic Probability Influences Motor Preparation Signals and Time to Saccadic Initiation , 1998, The Journal of Neuroscience.

[20]  D. Munoz,et al.  A neural correlate for the gap effect on saccadic reaction times in monkey. , 1995, Journal of neurophysiology.

[21]  D P Munoz,et al.  Saccadic reaction time in the monkey: advanced preparation of oculomotor programs is primarily responsible for express saccade occurrence. , 1996, Journal of neurophysiology.

[22]  Jan Theeuwes,et al.  The influence of distractors on express saccades. , 2017, Journal of vision.

[23]  Michele A Basso,et al.  Preparing to Move Increases the Sensitivity of Superior Colliculus Neurons , 2008, The Journal of Neuroscience.

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

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

[26]  R. Boch,et al.  Express-saccades of the monkey: Effect of daily training on probability of occurrence and reaction time , 2004, Experimental Brain Research.

[27]  Andrew Hollingworth,et al.  Visual Working Memory Modulates Rapid Eye Movements to Simple Onset Targets , 2013, Psychological science.

[28]  Laurent Itti,et al.  Linking visual response properties in the superior colliculus to saccade behavior , 2012, The European journal of neuroscience.

[29]  J. Barton,et al.  The temporal dynamics of the distractor in the global effect , 2016, Experimental Brain Research.

[30]  Martin Rolfs,et al.  Adaptive deployment of spatial and feature-based attention before saccades , 2013, Vision Research.

[31]  R. Klein,et al.  What are human express saccades? , 1993, Perception & psychophysics.

[32]  A. Fuchs,et al.  Further properties of the human saccadic system: eye movements and correction saccades with and without visual fixation points. , 1969, Vision research.

[33]  David L. Sparks,et al.  Movement fields of saccade-related burst neurons in the monkey superior colliculus , 1980, Brain Research.

[34]  Thomas P. Trappenberg,et al.  Spatial Interactions in the Superior Colliculus Predict Saccade Behavior in a Neural Field Model , 2012, Journal of Cognitive Neuroscience.

[35]  R. Wurtz,et al.  Saccade-related activity in monkey superior colliculus. II. Spread of activity during saccades. , 1995, Journal of neurophysiology.

[36]  J. Theeuwes,et al.  Distractors that signal reward attract the eyes , 2015 .

[37]  B. Fischer,et al.  Express-saccades of the monkey: Reaction times versus intensity, size, duration, and eccentricity of their targets , 2004, Experimental Brain Research.

[38]  P. Reuter-Lorenz,et al.  The reduction of saccadic latency by prior offset of the fixation point: An analysis of the gap effect , 1991, Perception & psychophysics.

[39]  Robert A. Marino,et al.  Spatial relationships of visuomotor transformations in the superior colliculus map. , 2008, Journal of neurophysiology.

[40]  J. Schall,et al.  Neural Control of Voluntary Movement Initiation , 1996, Science.

[41]  R. Wurtz,et al.  Modification of saccadic eye movements by GABA-related substances. I. Effect of muscimol and bicuculline in monkey superior colliculus. , 1985, Journal of neurophysiology.

[42]  G. Pari,et al.  Deficits in saccadic eye-movement control in Parkinson's disease , 2005, Neuropsychologia.

[43]  Jan Theeuwes,et al.  A competitive integration model of exogenous and endogenous eye movements , 2010, Biological Cybernetics.

[44]  M. Kokubun,et al.  Effects of age, intelligence and executive control function on saccadic reaction time in persons with intellectual disabilities. , 2011, Research in developmental disabilities.

[45]  David E. Irwin,et al.  Attentional capture and aging: implications for visual search performance and oculomotor control. , 1999, Psychology and aging.

[46]  Robert M. Boynton,et al.  Luminance as a Parameter of the Eye-Movement Control System* , 1967 .

[47]  John M. Findlay,et al.  Spatial and temporal factors in the predictive generation of saccadic eye movements , 1981, Vision Research.

[48]  Jay Pratt,et al.  Visual processing of targets can reduce saccadic latencies , 2005, Vision Research.

[49]  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.

[50]  D. Munoz,et al.  Competitive Integration of Visual and Preparatory Signals in the Superior Colliculus during Saccadic Programming , 2007, The Journal of Neuroscience.

[51]  Z. Kapoula,et al.  Long Latency and High Variability in Accuracy-Speed of Prosaccades in Alzheimer's Disease at Mild to Moderate Stage , 2011, Dementia and Geriatric Cognitive Disorders Extra.

[52]  K. Nakayama,et al.  The influence of object-relative visuomotor set on express saccades. , 2007, Journal of vision.

[53]  M. Saslow.  Effects of components of displacement-step stimuli upon latency for saccadic eye movement. , 1967, Journal of the Optical Society of America.

[54]  M. Albert,et al.  The effect of increasing age on the latency for saccadic eye movements. , 1983, Journal of gerontology.

[55]  Robert A. Marino,et al.  The effects of bottom-up target luminance and top-down spatial target predictability on saccadic reaction times , 2009, Experimental Brain Research.

[56]  J. Theeuwes,et al.  The time course of top-down control on saccade averaging , 2014, Vision Research.

[57]  B. Breitmeyer,et al.  Mechanisms of visual attention revealed by saccadic eye movements , 1987, Neuropsychologia.

[58]  P. E. Hallett,et al.  Retinal eccentricity and the latency of eye saccades , 1994, Vision Research.

[59]  R. H. S. Carpenter,et al.  Neural computation of log likelihood in control of saccadic eye movements , 1995, Nature.

[60]  B. Fischer,et al.  Saccadic eye movements after extremely short reaction times in the monkey , 1983, Brain Research.

[61]  Petroc Sumner,et al.  Temporal dynamics of saccadic distraction. , 2009, Journal of vision.

[62]  B. Fischer,et al.  Human express saccades: extremely short reaction times of goal directed eye movements , 2004, Experimental Brain Research.

[63]  Petroc Sumner,et al.  Determinants of saccade latency , 2011 .

[64]  J. Badler,et al.  Anticipatory Movement Timing Using Prediction and External Cues , 2006, The Journal of Neuroscience.

[65]  P. E. Hallett,et al.  Dependence of saccadic eye-movements on stimulus luminance, and an effect of task , 1988, Vision Research.

[66]  A. C. Smit,et al.  A short-latency transition in saccade dynamics during square-wave tracking and its significance for the differentiation of visually-guided and predictive saccades , 2004, Experimental Brain Research.

[67]  C. Reekum,et al.  Eye spy with my little eye: Motivational relevance of visual stimuli guide eye-movements at different processing stages , 2017, Biological Psychology.

[68]  P. Sterzer,et al.  The influence of motivational salience on saccade latencies , 2012, Experimental Brain Research.

[69]  M. Donk,et al.  The effects of saccade-contingent changes on oculomotor capture: salience is important even beyond the first oculomotor response , 2014, Attention, perception & psychophysics.

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

[71]  D. Munoz,et al.  Age-related trends in saccade characteristics among the elderly , 2011, Neurobiology of Aging.

[72]  Robert A. Marino,et al.  Linking express saccade occurance to stimulus properties and sensorimotor integration in the superior colliculus. , 2015, Journal of neurophysiology.

[73]  Heiner Deubel,et al.  Inhibition of saccades elicits attentional suppression. , 2013, Journal of vision.

[74]  Robin Walker,et al.  Control of voluntary and reflexive saccades , 2000, Experimental Brain Research.

[75]  Elizabeth L Irving,et al.  Horizontal saccade dynamics across the human life span. , 2006, Investigative ophthalmology & visual science.

[76]  Wieske van Zoest,et al.  The oculomotor salience of flicker, apparent motion and continuous motion in saccade trajectories , 2016, Experimental Brain Research.

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

[78]  J. Findlay,et al.  Express saccades: is there a separate population in humans? , 2004, Experimental Brain Research.