Accurate bidirectional saccade control by a single hemicortex.

Anatomical, electrophysiological and lesion studies indicate that each cortical hemisphere normally generates saccades directed to the contralateral side. In contrast, in patients who had an entire cortical hemisphere removed surgically (hemidecortication), the remaining hemicortex can generate both contraversive and ipsiversive saccades. However, current evidence indicates that ipsiversive saccades are grossly inaccurate. The obvious reason for this is that hemidecorticate patients are blind in the hemifield ipsilateral to the remaining hemicortex, and therefore normal visual signals are not available to drive ipsiversive saccades. However, absent vision also implies that visual error signals are not available to calibrate ipsiversive movements. Furthermore, the innate anatomical substrate needed to support accurate ipsiversive saccade control, in addition to the normal contraversive control, appears sparse. We show here that, in spite of these obstacles, hemidecorticate patients could generate accurate ipsiversive saccades in a task that dissociated hemianopia from saccade direction. In this task, while the patients fixated a central fixation target (FT), saccade targets (STs) were briefly presented to the intact visual hemifield contralateral to the intact hemicortex. The FT was then moved towards and beyond the former location of the ST which evoked tracking eye movements that moved the eyes towards and then beyond the ST, thereby moving the goal, ST, into the blind visual hemifield ipsilateral to the intact hemicortex. When the FT was extinguished, the patients generated, in the dark, ipsiversive saccades that moved their eyes to the remembered location of the ST with the same accuracy as normal control subjects. This indicates that a single hemicortex can mediate accurate bidirectional saccade control via fully functional bilateral connections from cortex to brainstem oculomotor structures. The mechanisms whereby visual signals can calibrate ipsiversive saccades remain elusive.

[1]  D. Boire,et al.  Anatomical sparing in the superior colliculus of hemispherectomized monkeys , 2001, Brain Research.

[2]  Y Agid,et al.  Cortical control of reflexive visually-guided saccades. , 1991, Brain : a journal of neurology.

[3]  R. Andersen,et al.  Electrical microstimulation distinguishes distinct saccade-related areas in the posterior parietal cortex. , 1998, Journal of neurophysiology.

[4]  M. Perenin,et al.  Visual function within the hemianopic field following early cerebral hemidecortication in man—I. Spatial localization , 1978, Neuropsychologia.

[5]  K Ohtsuka Properties of memory-guided saccades toward targets flashed during smooth pursuit in human subjects. , 1994, Investigative ophthalmology & visual science.

[6]  R. Douglas,et al.  Frontal lobe lesions in man cause difficulties in suppressing reflexive glances and in generating goal-directed saccades , 2004, Experimental Brain Research.

[7]  B. Troost,et al.  Hemispheric control of eye movements. II. Quantitative analysis of smooth pursuit in a hemispherectomy patient. , 1972, Archives of neurology.

[8]  D Guitton,et al.  Human head-free gaze saccades to targets flashed before gaze-pursuit are spatially accurate. , 1998, Journal of neurophysiology.

[9]  C. Pierrot-Deseilligny,et al.  Effects of cortical lesions on saccadic: eye movements in humans. , 2002, Annals of the New York Academy of Sciences.

[10]  Christoph J. Ploner,et al.  Effects of Cortical Lesions on Saccadic , 2002 .

[11]  J Schlag,et al.  Primate supplementary eye field: I. Comparative aspects of mesencephalic and pontine connections , 1990, The Journal of comparative neurology.

[12]  Edward J. Tehovnik,et al.  The dorsomedial frontal cortex of the rhesus monkey: topographic representation of saccades evoked by electrical stimulation , 2004, Experimental Brain Research.

[13]  D. Hovda,et al.  Development of a crossed corticotectal pathway following cerebral hemispherectomy in cats: a quantitative study of the projecting neurons. , 1995, Brain research. Developmental brain research.

[14]  W. Heide,et al.  Cortical control of double‐step saccades: Implications for spatial orientation , 1995, Annals of neurology.

[15]  M. Goldberg,et al.  Saccadic dysmetria in a patient with a right frontoparietal lesion. The importance of corollary discharge for accurate spatial behaviour. , 1992, Brain : a journal of neurology.

[16]  W. Fries,et al.  Contralateral cortical projections to the superior colliculus in the macaque monkey , 2004, Experimental Brain Research.

[17]  Lance M. Optican,et al.  Unix-based multiple-process system, for real-time data acquisition and control , 1982 .

[18]  C. J. McGrath,et al.  Effect of exchange rate return on volatility spill-over across trading regions , 2012 .

[19]  F R Robinson,et al.  Visual error is the stimulus for saccade gain adaptation. , 2001, Brain research. Cognitive brain research.

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

[21]  H. Jasper,et al.  Epilepsy and the functional anatomy of the human brain , 1985 .

[22]  J. Corvera,et al.  Oculomotor and oculovestibular functions in a hemispherectomy patient. , 1980, Archives of neurology.

[23]  G. Leichnetz,et al.  The prefrontal corticotectal projection in the monkey; An anterograde and retrograde horseradish peroxidase study , 1981, Neuroscience.

[24]  A. Fuchs,et al.  Saccadic gain modification: visual error drives motor adaptation. , 1998, Journal of neurophysiology.

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

[26]  T. Rasmussen,et al.  Functional Hemispherectomy in Children , 1993, Neuropediatrics.

[27]  K. Hepp,et al.  Frontal eye field projection to the paramedian pontine reticular formation traced with wheat germ agglutinin in the monkey , 1985, Brain Research.

[28]  C. Pierrot-Deseilligny,et al.  Impairment of extraretinal eye position signals after central thalamic lesions in humans , 2004, Experimental Brain Research.

[29]  S G Lisberger,et al.  Properties of signals that determine the amplitude and direction of saccadic eye movements in monkeys. , 1986, Journal of neurophysiology.

[30]  R. Wurtz,et al.  A Pathway in Primate Brain for Internal Monitoring of Movements , 2002, Science.

[31]  Nick Fogt,et al.  The Neurology of Eye Movements, 3rd ed. , 2000 .

[32]  L F Dell'Osso,et al.  Saccades to remembered targets: the effects of smooth pursuit and illusory stimulus motion. , 1996, Journal of neurophysiology.

[33]  A. Cowey,et al.  Blindsight in man and monkey. , 1997, Brain : a journal of neurology.

[34]  B. Gaymard,et al.  Eye movement disorders after frontal eye field lesions in humans , 2004, Experimental Brain Research.

[35]  L A Krubitzer,et al.  Frontal eye field as defined by intracortical microstimulation in squirrel monkeys, owl monkeys, and macaque monkeys II. cortical connections , 1986, The Journal of comparative neurology.

[36]  G. Leichnetz,et al.  Cortical projections to the paramedian tegmental and basilar pons in the monkey , 1984, The Journal of comparative neurology.

[37]  M. Gazzaniga,et al.  Bidirectional control of saccadic eye movements by the disconnected cerebral hemispheres , 2004, Experimental Brain Research.

[38]  R. Leigh,et al.  The neurology of eye movements , 2006 .

[39]  R. Tusa,et al.  Effect of unilateral cerebral cortical lesions on ocular motor behavior in monkeys: saccades and quick phases. , 1986, Journal of neurophysiology.

[40]  B. Troost,et al.  Hemispheric control of eye movements. I. Quantitative analysis of refixation saccades in a hemispherectomy patient. , 1972, Archives of neurology.

[41]  F. Robinson,et al.  Non-visual information does not drive saccade gain adaptation in monkeys , 2002, Brain Research.

[42]  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.

[43]  M. Schlag-Rey,et al.  Evidence for a supplementary eye field. , 1987, Journal of neurophysiology.

[44]  R. Wurtz,et al.  Visual and oculomotor functions of monkey substantia nigra pars reticulata. III. Memory-contingent visual and saccade responses. , 1983, Journal of neurophysiology.

[45]  D. Zee,et al.  Oculomotor function in the rhesus monkey after deafferentation of the extraocular muscles , 2001, Experimental Brain Research.

[46]  B. Gaymard,et al.  Cortical control of memory-guided saccades in man , 2004, Experimental Brain Research.

[47]  John H. R. Maunsell,et al.  The effect of frontal eye field and superior colliculus lesions on saccadic latencies in the rhesus monkey. , 1987, Journal of neurophysiology.

[48]  M. Schlag-Rey,et al.  Saccades can be aimed at the spatial location of targets flashed during pursuit. , 1990, Journal of neurophysiology.

[49]  T Paus,et al.  Blindsight in hemispherectomized patients as revealed by spatial summation across the vertical meridian. , 1997, Brain : a journal of neurology.

[50]  D. Sparks,et al.  Corollary discharge provides accurate eye position information to the oculomotor system. , 1983, Science.

[51]  M. Schlag-Rey,et al.  The frontal eye field provides the goal of saccadic eye movement , 2004, Experimental Brain Research.

[52]  R.N.Dej.,et al.  Epilepsy and the Functional Anatomy of the Human Brain , 1954, Neurology.

[53]  C Pierrot-Deseilligny,et al.  Cortical control of saccades in man. , 1991, Acta neurologica Belgica.

[54]  J. Sharpe,et al.  Control of the saccadic and smooth pursuit systems after cerebral hemidecortication. , 1979, Brain : a journal of neurology.

[55]  T Mergner,et al.  Saccadic reaction times in patients with frontal and parietal lesions. , 1992, Brain : a journal of neurology.

[56]  J. Bruell,et al.  Eye movements in an adult with cerebral hemispherectomy. , 1956, American journal of ophthalmology.

[57]  J Tanji,et al.  Microstimulation of the lateral wall of the intraparietal sulcus compared with the frontal eye field during oculomotor tasks. , 1999, Journal of neurophysiology.