Bidirectional and asymmetric smooth pursuit deficits in childhood hemispherectomy patients

Abstract

The neural circuitry engaged in supporting eye movements has been well characterized, but fundamental questions remain about the necessity and sufficiency of the individual hemispheric contributions. To gain a better understanding of the neural correlates of oculomotor control, we measured horizontal smooth pursuit tracking behavior in 14 patients following childhood hemispherectomy. Relative to developmentally typical age-matched controls, patients exhibited a bilateral and asymmetric pursuit deficit with reduced ipsilesional but elevated contralesional eye speeds, and asymmetric accompanying ‘catch up’ saccades. The atypical pursuit behavior could not be explained by a sensory deficit associated with their hemianopia, as patients adjusted their eye position to maintain visibility of the target. The pursuit deficit was also not accounted for by a general motor impairment as patients made faster catch-up saccades than controls, particularly in the ipsilesional direction. These results, all of which hold irrespective of whether the right or left hemisphere is resected, demonstrate that patients can compensate for reduced pursuit speeds by modulating their saccade characteristics. Overall, this study represents the most comprehensive characterization of smooth pursuit disturbances in hemispherectomy patients. Our results elucidate: 1) the competence of a single hemisphere for generating pursuit and compensatory behaviors; 2) the lack of a hemispheric bias supporting pursuit given large-scale cortical disruptions; and 3) that intact horizontal pursuit likely requires the interaction of brain circuitry across both hemispheres.