Oculomotor control after hemidecortication: a single hemisphere encodes corollary discharges for bilateral saccades

Patients who have had a cerebral hemisphere surgically removed as adults can generate accurate leftward and rightward saccadic eye movements, a task classically thought to require two hemispheres each controlling contralateral saccades. Here, we asked whether one hemisphere can generate sequences of saccades, the success of which requires the use of corollary discharges. Using a double-step saccade paradigm, we tested two hemidecorticate subjects who, by definition, are contralesionally hemianopic. In experiment 1, two targets, T1 and T2, were flashed in their seeing hemifield and subjects had to look in the dark to T1, then T2. In experiment 2, only one target was flashed; before looking at it, the subject had first to saccade voluntarily elsewhere. Both subjects were able to complete the tasks, independent of first and second saccade direction and whether the saccades were voluntarily or visually triggered. Both subjects displayed a strategy, typical in hemianopia, of making multiple-step saccades and placing, at overall movement-end, the recalled locations of T1 and T2 on off-foveal locations in their seeing hemifield, in a retinal area typically spanning a 5-15° window, depending on the subject, trial type and target eccentricity. In summary, a single hemisphere monitored the amplitude and direction of the first multiple-step saccade sequence bilaterally, and combined this information with the recalled initial retinotopic location of T2 (no longer visible) to generate a correct target-directed second saccade sequence in the dark. Unexpectedly, our hemidecorticate subjects performed better on the double-step task than subjects with isolated unilateral parietal lesions, reported in the literature to have marked deficiencies in monitoring contralesional saccadic eye movements. Thus, plasticity-dependent mechanisms that lead to recovery of function after hemidecortication are different than those deployed after smaller lesions. This implies a reconsideration of the classical links between behavioural deficits and discrete cortical lesions.