Saccadic dysmetria in a patient with a right frontoparietal lesion. The importance of corollary discharge for accurate spatial behaviour.

Double-step experiments have demonstrated that retinotopic coding is inadequate to explain the spatial performance of the saccadic system. In such experiments a subject is asked to make two successive saccades to fixate two sequentially flashed targets each of which disappears before the first saccade. Despite the dissonance thus created between the retinal location of the second target and the saccade necessary to acquire it, normal humans and monkeys perform the task perfectly well. Single unit recording in monkeys indicates that neurons in the superior colliculus, frontal eye fields and in parietal cortex generate a spatially accurate signal during the performance of double-step saccades, which is thought to be obtained by combining a retinotopic signal with a signal corollary to the previous saccadic eye movement. We studied saccadic eye movements in a patient with a right fronto-parietal lesion using single- and double-step tasks. Single saccades into the left (contralesional) hemifield had longer latency and were hypometric relative to those into the right (ipsilesional) hemifield. Varying the initial orbital position had no effect on the latency and accuracy of saccades to left and right retinal stimuli. When the patient was asked to do a double-step task with targets flashed first into the right field and then into the left field, she performed well. When she was asked to do the same task with a target flashed first into the left field and then into the right field she made the first saccade correctly but never acquired the second target, even though this required her to make a saccade in the normal direction to a stimulus that appeared in the normal field. Such a deficit therefore cannot be one of retinotopic or spatial coding, nor can it be one of generating a certain direction of saccade. We suggest that the deficit is a failure of corollary discharge, the inability to register the amplitude and direction of a saccade into the contralesional field, and use that information to update the representation of the location of the next saccade target.

[1]  M. B. Bender,et al.  Spatial organization of visual perception following injury to the brain. , 1947, Archives of neurology and psychiatry.

[2]  D. Robinson,et al.  A METHOD OF MEASURING EYE MOVEMENT USING A SCLERAL SEARCH COIL IN A MAGNETIC FIELD. , 1963, IEEE transactions on bio-medical engineering.

[3]  R. Wurtz,et al.  Activity of superior colliculus in behaving monkey. II. Effect of attention on neuronal responses. , 1972, Journal of neurophysiology.

[4]  R. Wurtz,et al.  Activity of superior colliculus in behaving monkey. IV. Effects of lesions on eye movements. , 1972, Journal of neurophysiology.

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

[6]  P. E. Hallett,et al.  Saccadic eye movements to flashed targets , 1976, Vision Research.

[7]  L E Mays,et al.  Saccades are spatially, not retinocentrically, coded. , 1980, Science.

[8]  D L Robinson,et al.  Behavioral enhancement of visual responses of prestriate neurons of the rhesus monkey. , 1980, Investigative ophthalmology & visual science.

[9]  D. Robinson,et al.  Behavioral enhancement of visual responses in monkey cerebral cortex. I. Modulation in posterior parietal cortex related to selective visual attention. , 1981, Journal of neurophysiology.

[10]  William F. Hughes,et al.  Functional Basis of Ocular Motility Disorders , 1984 .

[11]  A M Graybiel,et al.  The differential projection of two cytoarchitectonic subregions of the inferior parietal lobule of macaque upon the deep layers of the superior colliculus , 1985, The Journal of comparative neurology.

[12]  E. Làdavas,et al.  Is the hemispatial deficit produced by right parietal lobe damage associated with retinal or gravitational coordinates? , 1987, Brain : a journal of neurology.

[13]  C. Pierrot-Deseilligny,et al.  Latencies of visually guided saccades in unilateral hemispheric cerebral lesions , 1987, Annals of neurology.

[14]  M E Goldberg,et al.  Frontal eye field efferents in the macaque monkey: I. Subcortical pathways and topography of striatal and thalamic terminal fields , 1988, The Journal of comparative neurology.

[15]  K. Fukushima,et al.  Disturbances of voluntary control of saccadic eye movements in schizophrenic patients , 1988, Biological Psychiatry.

[16]  D. Sparks,et al.  Population coding of saccadic eye movements by neurons in the superior colliculus , 1988, Nature.

[17]  C. Bruce,et al.  Frontal eye field efferents in the macaque monkey: II. Topography of terminal fields in midbrain and pons , 1988, The Journal of comparative neurology.

[18]  Richard A. Andersen,et al.  A back-propagation programmed network that simulates response properties of a subset of posterior parietal neurons , 1988, Nature.

[19]  J. Lynch,et al.  Deficits of visual attention and saccadic eye movements after lesions of parietooccipital cortex in monkeys. , 1989, Journal of neurophysiology.

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

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

[22]  P. Carpenter,et al.  Frames of reference for allocating attention to space: Evidence from the neglect syndrome , 1990, Neuropsychologia.

[23]  M. Goldberg,et al.  Representation of visuomotor space in the parietal lobe of the monkey. , 1990, Cold Spring Harbor symposia on quantitative biology.

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

[25]  J R Duhamel,et al.  The updating of the representation of visual space in parietal cortex by intended eye movements. , 1992, Science.