Dynamic combination of position and motion information when tracking moving targets.

To accurately foveate a moving target, the oculomotor system needs to estimate the position of the target at the saccade end, based on information about its position and ongoing movement, while accounting for neuronal delays and execution time of the saccade. We investigated human interceptive saccades and pursuit responses to moving targets defined by high and low luminance contrast or by chromatic contrast only (isoluminance). We used step-ramps with perpendicular directions between vertical target steps of 10 deg/s and horizontal ramps of 2.5 to 20 deg/s to separate errors with respect to the position step of the target in the vertical dimension, and errors related to target motion in the horizontal dimension. Interceptive saccades to targets of high and low luminance contrast landed close to the actual target positions, suggesting relatively accurate estimates of the amount of target displacement. Interceptive saccades to isoluminant targets were less accurate. They landed at positions the target had on average 100 ms before saccade onset. One account of this finding is that the integration of target motion is compromised for isoluminant targets moving in the periphery. In this case, the oculomotor system can use an accurate, but delayed position component, but cannot account for target movement. This deficit was also present for the postsaccadic pursuit speed. For the two luminance conditions, pursuit direction and speed were adjusted depending on the saccadic landing position. The rapid postsaccadic pursuit adjustments suggest shared position- and motion-related signals of target and eye for saccade and pursuit control.

[1]  Eileen Kowler,et al.  Davida Teller Award Lecture 2013: the importance of prediction and anticipation in the control of smooth pursuit eye movements. , 2014, Journal of vision.

[2]  Philippe Lefèvre,et al.  A dynamic representation of target motion drives predictive smooth pursuit during target blanking. , 2008, Journal of vision.

[3]  Ziad M Hafed,et al.  Superior Colliculus Inactivation Causes Stable Offsets in Eye Position during Tracking , 2008, The Journal of Neuroscience.

[4]  K. Kawano,et al.  Role of the pretectal nucleus of the optic tract in short-latency ocular following responses in monkeys , 2000, Experimental Brain Research.

[5]  Christopher C. Pack,et al.  Temporal dynamics of a neural solution to the aperture problem in visual area MT of macaque brain , 2001, Nature.

[6]  L. M. Optican,et al.  Oculomotor System: Models , 2009 .

[7]  T D Albright,et al.  The Contribution of Color to Motion Processing in Macaque Middle Temporal Area , 1999, The Journal of Neuroscience.

[8]  Jean Bullier,et al.  The Timing of Information Transfer in the Visual System , 1997 .

[9]  Denis G. Pelli,et al.  ECVP '07 Abstracts , 2007, Perception.

[10]  G. Barnes,et al.  The mechanism of prediction in human smooth pursuit eye movements. , 1991, The Journal of physiology.

[11]  Jérome Fleuriet,et al.  Saccadic Interception of a Moving Visual Target after a Spatiotemporal Perturbation , 2012, The Journal of Neuroscience.

[12]  Luis A. Lesmes,et al.  Perceptual motion standstill in rapidly moving chromatic displays. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[13]  Patrick Cavanagh,et al.  Cooperative interactions between saccadic and pursuit planning when targeting a moving object , 2017 .

[14]  Chih-Yang Chen,et al.  Sharper, Stronger, Faster Upper Visual Field Representation in Primate Superior Colliculus , 2016, Current Biology.

[15]  Eugene McSorley,et al.  The influence of spatial frequency and contrast on saccade latencies , 2004, Vision Research.

[16]  K. Gegenfurtner The Interaction Between Vision and Eye Movements † , 2016, Perception.

[17]  Alexander C. Schütz,et al.  Eye movements and perception: a selective review. , 2011, Journal of vision.

[18]  B Brown,et al.  The effect of target contrast variation on dynamic visual acuity and eye movements. , 1972, Vision research.

[19]  M. Hawken,et al.  Perceived velocity of luminance, chromatic and non-fourier stimuli: Influence of contrast and temporal frequency , 1996, Vision Research.

[20]  Laurent Itti,et al.  Color-Related Signals in the Primate Superior Colliculus , 2009, The Journal of Neuroscience.

[21]  Laurent Goffart,et al.  Does the Brain Extrapolate the Position of a Transient Moving Target? , 2015, The Journal of Neuroscience.

[22]  Michael E. Goldberg,et al.  Effect of stimulus position and velocity upon the maintenance of smooth pursuit eye velocity , 1994, Vision Research.

[23]  E Brenner,et al.  Perception and action are based on the same visual information: distinction between position and velocity. , 1995, Journal of experimental psychology. Human perception and performance.

[24]  S G Lisberger,et al.  Visual motion processing for the initiation of smooth-pursuit eye movements in humans. , 1986, Journal of neurophysiology.

[25]  A. Terry Bahill,et al.  Smooth pursuit eye movements in response to predictable target motions , 1983, Vision Research.

[26]  A. King,et al.  The superior colliculus , 2004, Current Biology.

[27]  Karl R Gegenfurtner,et al.  Dynamics of oculomotor direction discrimination. , 2012, Journal of vision.

[28]  Ulrich Büttner,et al.  Saccades to stationary and moving targets differ in the monkey , 2004, Experimental Brain Research.

[29]  N. Shimizu [Neurology of eye movements]. , 2000, Rinsho shinkeigaku = Clinical neurology.

[30]  Laurent Goffart,et al.  The caudal fastigial nucleus and the steering of saccades toward a moving visual target. , 2018, Journal of neurophysiology.

[31]  Leland S Stone,et al.  Oculometric assessment of dynamic visual processing. , 2014, Journal of vision.

[32]  Karl R Gegenfurtner,et al.  Effects of contrast on smooth pursuit eye movements. , 2005, Journal of vision.

[33]  R. Gellman,et al.  Motion processing for saccadic eye movements in humans , 2004, Experimental Brain Research.

[34]  D. Methling,et al.  Sehscharfe des auges bei horizontalen folgebewegungen , 1968 .

[35]  T D Albright,et al.  What happens if it changes color when it moves?: the nature of chromatic input to macaque visual area MT , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[36]  Simon Heywood,et al.  Saccades to step-ramp stimuli , 1981, Vision Research.

[37]  Philippe Lefèvre,et al.  Evidence for synergy between saccades and smooth pursuit during transient target disappearance. , 2006, Journal of neurophysiology.

[38]  Lance M. Optican,et al.  What stops a saccade? , 2017, Philosophical Transactions of the Royal Society B: Biological Sciences.

[39]  R. Krauzlis Recasting the smooth pursuit eye movement system. , 2004, Journal of neurophysiology.

[40]  C. Rashbass,et al.  The relationship between saccadic and smooth tracking eye movements , 1961, The Journal of physiology.

[41]  Karl R. Gegenfurtner,et al.  Temporal and chromatic properties of motion mechanisms , 1995, Vision Research.

[42]  Patrick Cavanagh,et al.  Dissociation between the Perceptual and Saccadic Localization of Moving Objects , 2015, Current Biology.

[43]  N. J. Gandhi,et al.  Motor functions of the superior colliculus. , 2011, Annual review of neuroscience.

[44]  Ioannis Agtzidis,et al.  In the pursuit of (ground) truth: a hand-labelling tool for eye movements recorded during dynamic scene viewing , 2016, 2016 IEEE Second Workshop on Eye Tracking and Visualization (ETVIS).

[45]  B Brown,et al.  Resolution thresholds for moving targets at the fovea and in the peripheral retina. , 1972, Vision research.

[46]  M. Hawken,et al.  Smooth pursuit eye movements to isoluminant targets. , 2008, Journal of neurophysiology.

[47]  M J Hawken,et al.  Pursuit eye movements to second-order motion targets. , 2001, Journal of the Optical Society of America. A, Optics, image science, and vision.

[48]  Dirk Kerzel,et al.  Visually guided movements to color targets , 2006, Experimental Brain Research.

[49]  Jean-Charles Quinton,et al.  Neurophysiology of visually guided eye movements: critical review and alternative viewpoint. , 2018, Journal of neurophysiology.

[50]  R J Krauzlis,et al.  Discharge properties of neurons in the rostral superior colliculus of the monkey during smooth-pursuit eye movements. , 2000, Journal of neurophysiology.

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

[52]  Karl R. Gegenfurtner,et al.  Execution of saccadic eye movements affects speed perception , 2018, Proceedings of the National Academy of Sciences.

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

[54]  P. Viviani,et al.  The curvature of oblique saccades , 1977, Vision Research.

[55]  Karl R Gegenfurtner,et al.  Color contributes to object-contour perception in natural scenes. , 2017, Journal of vision.

[56]  P. Cavanagh,et al.  A minimum motion technique for judging equiluminance , 1983 .

[57]  K. Gegenfurtner,et al.  Competition between color and luminance for target selection in smooth pursuit and saccadic eye movements. , 2008, Journal of vision.

[58]  D. Pélisson,et al.  On-line modification of saccadic eye movements by retinal signals , 2003, Neuroreport.

[59]  Pierre M. Daye,et al.  Switching between two targets with non‐constant velocity profiles reveals shared internal model of target motion , 2016, The European journal of neuroscience.

[60]  Gunnar Blohm,et al.  Direct evidence for a position input to the smooth pursuit system. , 2005, Journal of neurophysiology.

[61]  Eileen Kowler,et al.  Sensitivity of smooth eye movement to small differences in target velocity , 1987, Vision Research.

[62]  Karl R. Gegenfurtner,et al.  Contrast dependence of colour and luminance motion mechanisms in human vision , 1994, Nature.

[63]  Casimir J. H. Ludwig,et al.  Measuring saccade curvature: A curve-fitting approach , 2002, Behavior research methods, instruments, & computers : a journal of the Psychonomic Society, Inc.

[64]  Laurent Goffart,et al.  Synchronizing the tracking eye movements with the motion of a visual target: Basic neural processes. , 2017, Progress in brain research.

[65]  R. V. van Beers Saccadic Eye Movements Minimize the Consequences of Motor Noise , 2008, PloS one.

[66]  Gunnar Blohm,et al.  Catch-up saccades in head-unrestrained conditions reveal that saccade amplitude is corrected using an internal model of target movement. , 2014, Journal of vision.

[67]  W. Newsome,et al.  Deficits in visual motion processing following ibotenic acid lesions of the middle temporal visual area of the macaque monkey , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[68]  P. Thompson Perceived rate of movement depends on contrast , 1982, Vision Research.

[69]  M. Missal,et al.  Quantitative analysis of catch-up saccades during sustained pursuit. , 2002, Journal of neurophysiology.

[70]  S. Lisberger,et al.  Properties of visual inputs that initiate horizontal smooth pursuit eye movements in monkeys , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[71]  O. Braddick A short-range process in apparent motion. , 1974, Vision research.

[72]  Casper J. Erkelens,et al.  The Initial Direction and Landing Position of Saccades , 1995 .

[73]  R J Krauzlis,et al.  Activation and inactivation of rostral superior colliculus neurons during smooth-pursuit eye movements in monkeys. , 2000, Journal of neurophysiology.

[74]  Jacques Droulez,et al.  Target velocity based prediction in saccadic vector programming , 1989, Vision Research.

[75]  David A. Robinson,et al.  Models of the saccadic eye movement control system , 1973, Kybernetik.

[76]  E. Ludvigh,et al.  Study of visual acuity during the ocular pursuit of moving test objects. I. Introduction. , 1958, Journal of the Optical Society of America.

[77]  Karl R. Gegenfurtner,et al.  Object recognition during foveating eye movements , 2009, Vision Research.

[78]  J. Movshon,et al.  Chromatic properties of neurons in macaque MT , 1994, Visual Neuroscience.

[79]  Frank Bremmer,et al.  The Dorsal Visual System Predicts Future and Remembers Past Eye Position , 2016, Front. Syst. Neurosci..

[80]  Ziad M Hafed,et al.  Eye Position Error Influence over “Open-Loop” Smooth Pursuit Initiation , 2018, The Journal of Neuroscience.

[81]  E. Keller,et al.  Velocity prediction in corrective saccades during smooth-pursuit eye movements in monkey , 2004, Experimental Brain Research.

[82]  K C Engel,et al.  Oculomotor tracking in two dimensions. , 1999, Journal of neurophysiology.

[83]  D. W. Heeley,et al.  Cardinal directions of color space , 1982, Vision Research.

[84]  F Bremmer,et al.  Directional asymmetry of neurons in cortical areas MT and MST projecting to the NOT-DTN in macaques. , 2002, Journal of neurophysiology.

[85]  P. Thompson,et al.  Human speed perception is contrast dependent , 1992, Vision Research.

[86]  Gunnar Blohm,et al.  Weighted integration of short term memory and sensory signals in the oculomotor system , 2017, bioRxiv.

[87]  W. Bialek,et al.  A sensory source for motor variation , 2005, Nature.

[88]  Philippe Lefèvre,et al.  Asynchrony between position and motion signals in the saccadic system. , 2006, Journal of neurophysiology.

[89]  Laurent Goffart,et al.  Pursuit disorder and saccade dysmetria after caudal fastigial inactivation in the monkey. , 2018, Journal of neurophysiology.

[90]  Eileen Kowler Eye movements: The past 25years , 2011, Vision Research.

[91]  P. Lennie,et al.  Chromatic mechanisms in lateral geniculate nucleus of macaque. , 1984, The Journal of physiology.

[92]  Vincent P Ferrera,et al.  Neuronal responses to moving targets in monkey frontal eye fields. , 2008, Journal of neurophysiology.

[93]  E. Seidemann,et al.  Color Signals in Area MT of the Macaque Monkey , 1999, Neuron.

[94]  Aaron L Cecala,et al.  The superior colliculus and the steering of saccades toward a moving visual target , 2017, bioRxiv.

[95]  Laurent Perrinet,et al.  Saccadic foveation of a moving visual target in the rhesus monkey. , 2011, Journal of neurophysiology.

[96]  O E Favreau,et al.  Perceived velocity of moving chromatic gratings. , 1984, Journal of the Optical Society of America. A, Optics and image science.

[97]  Alexander Thiele,et al.  Chromatic sensitivity of neurones in area MT of the anaesthetised macaque monkey compared to human motion perception , 2005, Experimental Brain Research.

[98]  Iain D Gilchrist,et al.  The target velocity integration function for saccades. , 2010, Journal of vision.

[99]  B Brown,et al.  Dynamic visual acuity, eye movements and peripheral acuity for moving targets. , 1972, Vision research.

[100]  R. Krauzlis The Control of Voluntary Eye Movements: New Perspectives , 2005, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[101]  Stephen G Lisberger,et al.  Visual Guidance of Smooth Pursuit Eye Movements. , 2015, Annual review of vision science.

[102]  Jean-Jacques Orban de Xivry,et al.  Saccades and pursuit: two outcomes of a single sensorimotor process , 2007, The Journal of physiology.

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

[104]  S. Zeki,et al.  Response properties and receptive fields of cells in an anatomically defined region of the superior temporal sulcus in the monkey. , 1971, Brain research.

[105]  R. Gellman,et al.  Human smooth pursuit: stimulus-dependent responses. , 1987, Journal of neurophysiology.

[106]  Eli Brenner,et al.  Corrective saccades influence velocity judgments and interception , 2019, Scientific Reports.

[107]  R. Snowden,et al.  Speed perception fogs up as visibility drops , 1998, Nature.

[108]  W. Newsome,et al.  A selective impairment of motion perception following lesions of the middle temporal visual area (MT) , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[109]  P Cavanagh,et al.  Attention-based motion perception. , 1992, Science.

[110]  M. Schlag-Rey,et al.  Through the eye, slowly; Delays and localization errors in the visual system , 2002, Nature Reviews Neuroscience.

[111]  J. A. Gisbergen,et al.  An analysis of curvature in fast and slow human saccades , 2004, Experimental Brain Research.

[112]  Z L Lu,et al.  Three-systems theory of human visual motion perception: review and update. , 2001, Journal of the Optical Society of America. A, Optics, image science, and vision.

[113]  S. Wuerger,et al.  The perception of motion in chromatic stimuli. , 2005, Behavioral and cognitive neuroscience reviews.

[114]  Thomas Martinetz,et al.  Variability of eye movements when viewing dynamic natural scenes. , 2010, Journal of vision.

[115]  Karl R. Gegenfurtner,et al.  Precision of speed discrimination and smooth pursuit eye movements , 2009, Vision Research.

[116]  Bart Farell,et al.  Vernier acuity: Effects of chromatic content, blur and contrast , 1991, Vision Research.

[117]  N J Gandhi,et al.  Discharge of superior collicular neurons during saccades made to moving targets. , 1996, Journal of neurophysiology.

[118]  K. Tanaka,et al.  Directionally selective response of cells in the middle temporal area (MT) of the macaque monkey to the movement of equiluminous opponent color stimuli , 2004, Experimental Brain Research.

[119]  D L Sparks,et al.  Translation of sensory signals into commands for control of saccadic eye movements: role of primate superior colliculus. , 1986, Physiological reviews.

[120]  D. Ringach,et al.  Dynamics of smooth pursuit maintenance. , 2009, Journal of neurophysiology.