On the Visual Input Driving Human Smooth-Pursuit Eye Movements

Current computational models of smooth-pursuit eye movements assume that the primary visual input is local retinal-image motion (often referred to as retinal slip). However, we show that humans can pursue object motion with considerable accuracy, even in the presence of conflicting local image motion. This finding indicates that the visual cortical area(s) controlling pursuit must be able to perform a spatio-temporal integration of local image motion into a signal related to object motion. We also provide evidence that the object-motion signal that drives pursuit is related to the signal that supports perception. We conclude that current models of pursuit should be modified to include a visual input that encodes perceived object motion and not merely retinal image motion. Finally, our findings suggest that the measurement of eye movements can be used to monitor visual perception, with particular value in applied settings as this non-intrusive approach would not require interrupting ongoing work or training.

[1]  S. Yasui,et al.  Perceived visual motion as effective stimulus to pursuit eye movement system , 1975, Science.

[2]  W. Newsome,et al.  Directional pursuit deficits following lesions of the foveal representation within the superior temporal sulcus of the macaque monkey. , 1987, Journal of neurophysiology.

[3]  John H. R. Maunsell,et al.  The connections of the middle temporal visual area (MT) and their relationship to a cortical hierarchy in the macaque monkey , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  Arien Mack,et al.  Is perceived motion a stimulus for smooth pursuit , 1982, Vision Research.

[5]  A Mack,et al.  Smooth pursuit eye movements: is perceived motion necessary? , 1979, Science.

[6]  J. Movshon The velocity tuning of single units in cat striate cortex. , 1975, The Journal of physiology.

[7]  M. Shiffrar,et al.  Increased Motion Linking Across Edges with Decreased Luminance Contrast, Edge Width and Duration , 1996, Vision Research.

[8]  E. Adelson,et al.  The analysis of moving visual patterns , 1985 .

[9]  John H. R. Maunsell,et al.  Coding of image contrast in central visual pathways of the macaque monkey , 1990, Vision Research.

[10]  C. Bruce,et al.  Neural responses related to smooth-pursuit eye movements and their correspondence with electrically elicited smooth eye movements in the primate frontal eye field. , 1994, Journal of neurophysiology.

[11]  S Celebrini,et al.  Microstimulation of extrastriate area MST influences performance on a direction discrimination task. , 1995, Journal of neurophysiology.

[12]  F A Miles,et al.  Visual tracking and the primate flocculus. , 1975, Science.

[13]  Drake R. Bradley,et al.  The effect of smooth tracking and saccadic eye movements on the perception of size: The shrinking circle illusion , 1975, Vision Research.

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

[15]  Thomas D. Albright,et al.  Neural correlates of perceptual motion coherence , 1992, Nature.

[16]  Harry J. Wyatt,et al.  The role of perceived motion in smooth pursuit eye movements , 1979, Vision Research.

[17]  J. Sharpe,et al.  Deficits of smooth‐pursuit eye movement after unilateral frontal lobe lesions , 1995, Annals of neurology.

[18]  F. A. Miles,et al.  Long-term adaptive changes in primate vestibuloocular reflex. IV. Electrophysiological observations in flocculus of adapted monkeys. , 1980, Journal of neurophysiology.

[19]  E. L. Keller,et al.  Smooth-pursuit initiation in the presence of a textured background in monkey , 1986, Vision Research.

[20]  S. Lisberger,et al.  Visual responses of Purkinje cells in the cerebellar flocculus during smooth-pursuit eye movements in monkeys. I. Simple spikes. , 1990, Journal of neurophysiology.

[21]  F. A. Miles,et al.  Long-term adaptive changes in primate vestibuloocular reflex. III. Electrophysiological observations in flocculus of normal monkeys. , 1980, Journal of neurophysiology.

[22]  W. Merigan,et al.  Motion perception following lesions of the superior temporal sulcus in the monkey. , 1994, Cerebral cortex.

[23]  Leslie G. Ungerleider,et al.  Multiple visual areas in the caudal superior temporal sulcus of the macaque , 1986, The Journal of comparative neurology.

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

[25]  J. Sharpe,et al.  Retinotopic and directional deficits of smooth pursuit initiation after posterior cerebral hemispheric lesions , 1993, Neurology.

[26]  F A Miles,et al.  Effects of stationary textured backgrounds on the initiation of pursuit eye movements in monkeys. , 1992, Journal of neurophysiology.

[27]  R J Leigh,et al.  Two distinct deficits of visual tracking caused by unilateral lesions of cerebral cortex in humans , 1988, Annals of neurology.

[28]  H. Collewijn,et al.  Human smooth and saccadic eye movements during voluntary pursuit of different target motions on different backgrounds. , 1984, The Journal of physiology.

[29]  E. J. Morris,et al.  Different responses to small visual errors during initiation and maintenance of smooth-pursuit eye movements in monkeys. , 1987, Journal of neurophysiology.

[30]  D. A. Suzuki,et al.  Target velocity signals of visual tracking in vermal Purkinje cells of the monkey. , 1979, Science.

[31]  T. Albright Direction and orientation selectivity of neurons in visual area MT of the macaque. , 1984, Journal of neurophysiology.

[32]  D. Bradley The apparent size of the path traversed by a rotating target during saccadic and smooth pursuit: New data on the shrinking circle illusion , 1977 .

[33]  Maggie Shiffrar,et al.  The influence of terminators on motion integration across space , 1992, Vision Research.

[34]  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.

[35]  R. Wurtz,et al.  Recovery of function after lesions in the superior temporal sulcus in the monkey. , 1991, Journal of neurophysiology.

[36]  D. G. Albrecht,et al.  Motion selectivity and the contrast-response function of simple cells in the visual cortex , 1991, Visual Neuroscience.

[37]  S G Lisberger,et al.  Visual motion commands for pursuit eye movements in the cerebellum. , 1991, Science.

[38]  H. Komatsu,et al.  Modulation of pursuit eye movements by stimulation of cortical areas MT and MST. , 1989, Journal of neurophysiology.

[39]  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.

[40]  S G Lisberger,et al.  Simple spike responses of gaze velocity Purkinje cells in the floccular lobe of the monkey during the onset and offset of pursuit eye movements. , 1994, Journal of neurophysiology.

[41]  Dario L. Ringach,et al.  Binocular eye movements caused by the perception of three-Dimensional structure from motion , 1996, Vision Research.