A foveal target increases catch-up saccade frequency during smooth pursuit.

Images that move rapidly across the retina of the human eye blur because the retina has sluggish temporal dynamics. Voluntary smooth pursuit eye movements are modeled as matching object velocity to minimize retinal motion and prevent retinal blurring. However, "catch-up" saccades that are ubiquitous during pursuit interrupt it and disrupt clear vision. But catch-up saccades may not be a common feature of ocular pursuit, because their existence has been documented with a small moving spot, the classic pursuit stimulus, which is a weak motion stimulus that may poorly emulate larger pursuit objects. We found that spot pursuit does not generalize to that of larger objects. Observers pursued a spot or a larger virtual object with or without a superimposed spot target. Single-spot targets produced lower pursuit acceleration than larger objects. Critically, more saccadic intrusions occurred when stimuli had a central dot, even when position and velocity errors were equated, suggesting that catch-up saccades result from pursuing a single, small object or a feature on a large one. To determine what differentiates a large object from a small one, we progressively shrank the featureless virtual object and found that catch-up saccade frequency was highest when it fit in the fovea. The results suggest that pursuit of a small target or an object feature recruits a saccade mechanism that does not compensate for a weak motion signal; rather, the target compels foveation. Furthermore, catch-up saccades are likely generated by neural circuitry typically used to foveate small objects or features.

[1]  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.

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

[3]  W A Fletcher,et al.  Smooth pursuit dysfunction in Alzheimer's disease , 1988, Neurology.

[4]  J. Daléry,et al.  Poor performance in smooth pursuit and antisaccadic eye-movement tasks in healthy siblings of patients with schizophrenia , 2001, Psychiatry Research.

[5]  B. Dosher,et al.  The role of attention in the programming of saccades , 1995, Vision Research.

[6]  Y. Nakayama,et al.  The history of JOV of 10 years , 2008, J. Vis..

[7]  Jan Kassubek,et al.  Comparison of smooth pursuit eye movement deficits in multiple system atrophy and Parkinson’s disease , 2009, Journal of Neurology.

[8]  P. Thier,et al.  Eye movements of rhesus monkeys directed towards imaginary targets , 1999, Vision Research.

[9]  S G Lisberger,et al.  Postsaccadic enhancement of initiation of smooth pursuit eye movements in monkeys. , 1998, Journal of neurophysiology.

[10]  Martin J. Steinbach,et al.  Pursuing the perceptual rather than the retinal stimulus , 1976, Vision Research.

[11]  S. Watamaniuk,et al.  Motion Integration for Ocular Pursuit Does Not Hinder Perceptual Segregation of Moving Objects , 2014, The Journal of Neuroscience.

[12]  J. Meere The role of attention. , 2002 .

[13]  D. A. Suzuki,et al.  The role of the posterior vermis of monkey cerebellum in smooth-pursuit eye movement control. I. Eye and head movement-related activity. , 1988, Journal of neurophysiology.

[14]  W. Bialek,et al.  The Neural Basis for Combinatorial Coding in a Cortical Population Response , 2008, The Journal of Neuroscience.

[15]  R. McPeek,et al.  The eye dominates in guiding attention during simultaneous eye and hand movements. , 2011, Journal of vision.

[16]  N H Barmack,et al.  Dynamic visual acuity as an index of eye movement control. , 1970, Vision research.

[17]  E. L. Keller,et al.  Generation of smooth-pursuit eye movements: neuronal mechanisms and pathways , 1991, Neuroscience Research.

[18]  C W Tyler,et al.  Specific deficits of flicker sensitivity in glaucoma and ocular hypertension. , 1981, Investigative ophthalmology & visual science.

[19]  J. Horton The Neurobiology of Saccadic Eye Movements , 1990 .

[20]  K. H. Britten,et al.  Spatial Summation in the Receptive Fields of MT Neurons , 1999, The Journal of Neuroscience.

[21]  E. J. Morris,et al.  Visual motion processing and sensory-motor integration for smooth pursuit eye movements. , 1987, Annual review of neuroscience.

[22]  B. L. Zuber,et al.  Saccadic suppression: elevation of visual threshold associated with saccadic eye movements. , 1966, Experimental neurology.

[23]  Forrest L. Dimmick,et al.  The retina. The anatomy and the histology of the retina in man, ape, and monkey, including the consideration of visual functions, the history of physiological optics, and the histological laboratory technique. , 1944 .

[24]  Stephen G Lisberger,et al.  Visual Guidance of Smooth-Pursuit Eye Movements: Sensation, Action, and What Happens in Between , 2010, Neuron.

[25]  S G Lisberger,et al.  Partial ablations of the flocculus and ventral paraflocculus in monkeys cause linked deficits in smooth pursuit eye movements and adaptive modification of the VOR. , 2002, Journal of neurophysiology.

[26]  Ziad M. Hafed,et al.  Movements in Monkeys Colliculus Neurons During Smooth-Pursuit Eye Activation and Inactivation of Rostral Superior , 2015 .

[27]  S. Polyak,et al.  The retina : the anatomy and the histology of the retina in man, ape, and monkey, including the consideration of visual functions, the history of psysiological optics, and the histological laboratory technique , 1941 .

[28]  H Collewijn,et al.  Human fixation and pursuit in normal and open‐loop conditions: effects of central and peripheral retinal targets. , 1986, The Journal of physiology.

[29]  S. Liversedge,et al.  Saccadic eye movements and cognition , 2000, Trends in Cognitive Sciences.

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

[31]  D. A. Suzuki,et al.  The role of the posterior vermis of monkey cerebellum in smooth-pursuit eye movement control. II. Target velocity-related Purkinje cell activity. , 1988, Journal of neurophysiology.

[32]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

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

[34]  A. Fuchs,et al.  Discharge patterns of neurons in the pretectal nucleus of the optic tract (NOT) in the behaving primate. , 1990, Journal of neurophysiology.

[35]  R. Lencer,et al.  Role of anticipation and prediction in smooth pursuit eye movement control in Parkinson's disease , 2012, Movement disorders : official journal of the Movement Disorder Society.

[36]  G. Barnes,et al.  The influence of display characteristics on active pursuit and passively induced eye movements , 2004, Experimental Brain Research.

[37]  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.

[38]  M. Morgan,et al.  Efficiency of locating centres of dot-clusters by human observers , 1991, Vision Research.

[39]  H. Komatsu,et al.  Relation of cortical areas MT and MST to pursuit eye movements. II. Differentiation of retinal from extraretinal inputs. , 1988, Journal of neurophysiology.

[40]  R. Leigh,et al.  The neurology of eye movements , 1984 .

[41]  Zhenlan Jin,et al.  Flexibility of foveal attention during ocular pursuit. , 2011, Journal of vision.

[42]  C. Bruce,et al.  Smooth-pursuit eye movement representation in the primate frontal eye field. , 1991, Cerebral cortex.

[43]  J. L. Gordon,et al.  A model of the smooth pursuit eye movement system , 1986, Biological Cybernetics.

[44]  S. McKee,et al.  The detection of motion in the peripheral visual field , 1984, Vision Research.

[45]  H. Komatsu,et al.  Relation of cortical areas MT and MST to pursuit eye movements. I. Localization and visual properties of neurons. , 1988, Journal of neurophysiology.

[46]  R. Leigh,et al.  THE NEUROLOGY OF EYE MOVEMENTS FOURTH EDITION , 2006 .

[47]  M. Missal,et al.  What triggers catch-up saccades during visual tracking? , 2002, Journal of Neurophysiology.

[48]  M. Roth A quantitative assessment , 1987 .

[49]  Houeto Jean-Luc [Parkinson's disease]. , 2022, La Revue du praticien.

[50]  R. Wurtz,et al.  The Neurobiology of Saccadic Eye Movements , 1989 .

[51]  S. McKee,et al.  Visual acuity in the presence of retinal-image motion. , 1975, Journal of the Optical Society of America.

[52]  Harry J. Wyatt,et al.  Smooth pursuit eye movements with imaginary targets defined by extrafoveal cues , 1994, Vision Research.

[53]  R. Wurtz,et al.  Pursuit and optokinetic deficits following chemical lesions of cortical areas MT and MST. , 1988, Journal of neurophysiology.

[54]  L. A. Abel,et al.  Quantitative assessment of smooth pursuit gain and catch-up saccades in schizophrenia and affective disorders , 1991, Biological Psychiatry.

[55]  Stephen J Heinen,et al.  Human smooth pursuit direction discrimination , 1999, Vision Research.

[56]  S. G. Lisberger,et al.  A Control Systems Model of Smooth Pursuit Eye Movements with Realistic Emergent Properties , 1989, Neural Computation.

[57]  G. Zaccara,et al.  Smooth-pursuit eye movements: alterations in Alzheimer's disease , 1992, Journal of the Neurological Sciences.

[58]  S. Heinen Single neuron activity in the dorsomedial frontal cortex during smooth pursuit eye movements , 2004, Experimental Brain Research.

[59]  Robert M. Steinman,et al.  The effect of luminance on human smooth pursuit of perifoveal and foveal targets , 1978, Vision Research.

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

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

[62]  H. Komatsu,et al.  Relation of cortical areas MT and MST to pursuit eye movements. III. Interaction with full-field visual stimulation. , 1988, Journal of neurophysiology.

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

[64]  D G Pelli,et al.  The VideoToolbox software for visual psychophysics: transforming numbers into movies. , 1997, Spatial vision.

[65]  A. Mikami,et al.  Discharges of neurons in the dorsal paraflocculus of monkeys during eye movements and visual stimulation. , 1986, Journal of neurophysiology.

[66]  R M Steinman,et al.  Tracking eye movements with and without saccadic correction. , 1969, Vision research.