Visual-vestibular interaction in a bilateral model of the rotational and translational vestibulo-ocular reflexes : an investigation of viewing-context-dependent reflex performance

Traditionally, the vestibulo-ocular reflex (VOR) has been considered a stereotyped ocular counterrotation response to head movement that stabilizes a visual image on the retinae. However, during natural head movements, the appropriate magnitudes and directions of compensatory ocular deviations depend on viewing context. Moment-to-moment adjustments in VOR performance are required as gaze is redirected towards different viewing locations.This thesis presents an investigation of viewing-context-dependent VOR performance through the development of a physiologically and anatomically based bilateral model structure. Previous theoretical studies of visual-vestibular interactions during head-centered rotation are extended by simulating both ocular responses and those of individual premotor brainstem neuron types in an integrated binocular controller for slow eye movements. Central sensitivities to vestibular canal signals are modulated as a function of instantaneous binocular fixation state to simulate appropriate viewing-location-dependent changes in monocular rotational VOR performance and distinct premotor cell behaviors.A new hypothesis for the central dynamic processing of sensory otolith signals in the translational VOR is presented. Previous proposals suggested that the unique dynamic characteristics of otolith and canal afferent signals imply additional central processing in the translational as compared to the rotational VOR pathways. The strategy presented here demonstrates that projecting canal and otolith signals onto a shared premotor circuit at unique sites is sufficient to reproduce observed ocular and central behaviors without introducing additional central filters. By implementing this simple strategy in the bilateral model structure the ability to achieve appropriate compensatory responses for different translation directions and viewing locations in the horizontal plane is demonstrated.Finally, the model is extended to incorporate brainstem-cerebellar interactions. Current conclusions surrounding potential central sites for plasticity underlying long-term VOR gain adaptation are evaluated. The work makes new suggestions for vestibulo-ocular system organization and proposes directions for experimental work in addressing the following general themes: (1) Sensory convergence onto a shared premotor controller; (2) The role of a bilateral topology in motor pattern selection and binocular coordination; (3) The role of central connectivity in the appearance of distinct premotor cell types; (4) The ability to localize central sites for modifications underlying viewing-location-dependent and long-term adaptive changes in reflex performance