Context-dependence of the binocular VOR; an emerging property of brainstem circuit topology

The study of binocular control systems has unmasked several advantages linked to the topology of premotor neural networks. In the angular vestibulo-ocular reflex (VOR), there is a need to tune the gain of the reflex separately for each eye with head perturbations, depending on the distance and eccentricity of a visual target from the midsaggital plane of the head. The natural structural symmetry of the ocular premotor circuits can imbed the required changes in simultaneous vergence and conjugate components of the binocular VOR system. Here we demonstrate that including simple nonlinearities on the function of premotor cells in this symmetric circuit achieves the desired context-dependence for the binocular VOR. This approach allows very complex behaviors in response to sensory patterns without resorting to currently assumed complex cortical computations. The local premotor topology with its nonlinear properties can be sufficient for on-line reflex adaptation to behavioral context in the ocular system and has implications for other motor systems (such as stretch reflex modulation during rhythmic walking).