The Horizontal Angular Vestibulo-Ocular Reflex: A Nonlinear Mechanism for Context-Dependent Responses

Studies of the vestibulo-ocular reflex (VOR) have revealed that this type of involuntary eye movement is influenced by viewing distance. This paper presents a bilateral model for the horizontal angular VOR in the dark based on realistic physiological mechanisms. It is shown that by assigning proper nonlinear neural computations at the premotor level, the model is capable of replicating target-distance-dependent VOR responses that are in agreement with geometrical requirements. Central premotor responses in the model are also shown to be consistent with experimental observations. Moreover, the model performance after simulated unilateral canal plugging also reproduces experimental observations, an emerging property. Such local nonlinear computations could similarly generate context-dependent behaviors in other more complex motor systems.

I. Introduction

The vestibulo-ocular reflex (VOR) is a type of involuntary eye movement that stabilizes retinal images during head perturbations to maintain clear vision. As in any sensory-motor circuit, the VOR has three parts: 1) a sensory device to drive the system; 2) a central processing stage that combines sensory and motor feedback signals to generate motor commands based on a specific goal; and 3) a neuromuscular plant that produces the desired output. The vestibular apparatus consists of the semicircular canals and the otolith organs which detect head movements during the angular and translational motion, respectively. Circuits in the brainstem, including the vestibular nuclei (VN) and prepositus hypoglossi (PH), act as the main system controller to integrate the sensory drive and eye position information and provide motor neurons with proper commands. Motor neurons in turn activate the extraocular muscles that apply torques on the eyeball and produce rotational eye movements. These three rather simple sensory-motor components constitute the main VOR path, the so-called three neuron arc [1].