Colliding saccades evoked by frontal eye field stimulation: artifact or evidence for an oculomotor compensatory mechanism underlying double-step saccades?

Abstract. What happens when the goal is changed before the movement is executed? Both the double-step and colliding saccade paradigms address this issue as they introduce a discrepancy between the retinal images of targets in space and the commands generated by the oculomotor system necessary to attain those targets. To maintain spatial accuracy under such conditions, transformations must update ‘retinal error’ as eye position changes, and must also accommodate neural transmission delays in the system so that retinal and eye position information are temporally aligned. Different hypotheses have been suggested to account for these phenomena, based on observations of dissociable cortical and subcortical compensatory mechanisms. We now demonstrate how a single compensatory mechanism can be invoked to explain both double-step and colliding saccade paradigm results, based on the use of a damped signal of change in position that is used in both cases to update retinal error and, thereby, account for intervening movements. We conclude that the collision effect is not an artifact, but instead reveals a compensatory mechanism for saccades whose targets appear near the onset of a preceding saccade.

[1]  Peter Ford Dominey,et al.  A model of the cerebellum in adaptive control of saccadic gain , 1996, Biological cybernetics.

[2]  M. J. Nichols,et al.  Nonstationary properties of the saccadic system: new constraints on models of saccadic control. , 1995, Journal of neurophysiology.

[3]  Leslie G. Ungerleider,et al.  Dissociation of object and spatial visual processing pathways in human extrastriate cortex. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[4]  Richard A. Andersen,et al.  Sensorimotor transformation during eye movements to remembered visual targets , 1991, Vision Research.

[5]  M. Goldberg,et al.  Functional properties of corticotectal neurons in the monkey's frontal eye field. , 1987, Journal of neurophysiology.

[6]  E. L. Keller,et al.  Microstimulation of the primate cerebellar vermis during saccadic eye movements , 1983, Brain Research.

[7]  Michael I. Jordan,et al.  A more biologically plausible learning rule for neural networks. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[8]  C. Bruce,et al.  Primate frontal eye fields. III. Maintenance of a spatially accurate saccade signal. , 1990, Journal of neurophysiology.

[9]  H. Noda.  Cerebellar control of saccadic eye movements: its neural mechanisms and pathways. , 1991, The Japanese journal of physiology.

[10]  D L Sparks,et al.  Spatial localization of saccade targets. II. Activity of superior colliculus neurons preceding compensatory saccades. , 1983, Journal of neurophysiology.

[11]  Paul Dassonville,et al.  The use of egocentric and exocentric location cues in saccadic programming , 1995, Vision Research.

[12]  J. Schlag,et al.  Illusory localization of stimuli flashed in the dark before saccades , 1995, Vision Research.

[13]  H. Noda,et al.  Effects of fastigial stimulation upon visually-directed saccades in macaque monkeys , 1991, Neuroscience Research.

[14]  D L Robinson,et al.  Modified saccades evoked by stimulation of the macaque superior colliculus account for properties of the resettable integrator. , 1995, Journal of neurophysiology.

[15]  M. Schlag-Rey,et al.  Direction Constancy in the Oculomotor System , 1993 .

[16]  D. Sparks,et al.  Spatial localization of saccade targets. I. Compensation for stimulation-induced perturbations in eye position. , 1983, Journal of neurophysiology.

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

[18]  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.

[19]  D. Sparks,et al.  Dissociation of visual and saccade-related responses in superior colliculus neurons. , 1980, Journal of neurophysiology.

[20]  C. Scudder.  A new local feedback model of the saccadic burst generator. , 1988, Journal of neurophysiology.

[21]  L. Fogassi,et al.  Eye position effects on visual, memory, and saccade-related activity in areas LIP and 7a of macaque , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[22]  Johan Van Rensbergen,et al.  Visual and oculomotor functions : advances in eye movement research , 1994 .

[23]  P Dassonville,et al.  Oculomotor localization relies on a damped representation of saccadic eye displacement in human and nonhuman primates , 1992, Visual Neuroscience.

[24]  Michael E. Goldberg,et al.  Physiology of the frontal eye fields , 1984, Trends in Neurosciences.

[25]  K. Ohtsuka,et al.  The effect of microstimulation of the oculomotor vermis on discharges of fastigial neurons and visually-directed saccades in macaques , 1991, Neuroscience Research.

[26]  Peter Ford Dominey,et al.  A cortico-subcortical model for generation of spatially accurate sequential saccades. , 1992, Cerebral cortex.

[27]  M. Schlag-Rey,et al.  Colliding saccades may reveal the secret of their marching orders , 1990, Trends in Neurosciences.

[28]  P. E. Hallett,et al.  Saccadic eye movements towards stimuli triggered by prior saccades , 1976, Vision Research.

[29]  R. Andersen,et al.  Saccade-related activity in the lateral intraparietal area. II. Spatial properties. , 1991, Journal of neurophysiology.

[30]  D. Robinson.  Eye movements evoked by collicular stimulation in the alert monkey. , 1972, Vision research.

[31]  Paul Dassonville,et al.  For and Against Spatial Coding of Saccades , 1994 .

[32]  M. Schlag-Rey,et al.  How the frontal eye field can impose a saccade goal on superior colliculus neurons. , 1992, Journal of neurophysiology.