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A reevaluation of the vestibulo-ocular reflex

New ideas of its purpose, properties, neural substrate, and disorders

Department of Neurology, University Hospitals, and Department of Veterans Affairs Medical Center, Case Western Reserve University (Dr. Leigh), Cleveland, OH; and the Department of Neurology, Klinikum Grosshadern, Ludwig-Maximilians University (Dr. Brandt), Munich, Germany.

Conventional views of the vestibulo-ocular reflex (VOR) have emphasized testing with caloric stimuli and by passively rotating patients at low frequencies in a chair. The properties of the VOR tested under these conditions differ from the performance of this reflex during the natural function for which it evolved–locomotion. Only the VOR (and not visually mediated eye movements) can cope with the high-frequency angular and linear perturbations of the head that occur during locomotion; this is achieved by generating eye movements at short latency (<16 msec). Interpretation of vestibular testing is enhanced by the realization that, although the di- and trisynaptic components of the VOR are essential for this short-latency response, the overall accuracy and plasticity of the VOR depend upon a distributed, parallel network of neurons involving the vestibular nuclei. Neurons in this network variously encode inputs from the labyrinthine semicircular canals and otoliths, as well as from the visual and somatosensory systems. The central vestibular pathways branch to contact vestibular cortex (for perception) and the spinal cord (for control of posture). Thus, the vestibular nuclei basically coordinate the stabilization of gaze and posture, and contribute to the perception of verticality and self-motion. Consequently, brainstem disorders that disrupt the VOR cause not just only nystagmus, but also instability of posture (eg, increased fore-aft sway in patients with downbeat nystagmus) and disturbance of spatial orientation (eg, tilt of the subjective visual vertical in Wallenberg's syndrome).

Address correspondence and reprint requests to Dr. R. John Leigh, Department of Neurology, University Hospitals of Cleveland, 2074 Abington Road, Cleveland, OH 44106.

Supported in part by USPHS grant EY06717, NASA grant NAG9-571, the Office of Research and Development, Medical Research Service, Department of Veterans Affairs, and the Evenor Armington Fund (Dr. Leigh), and the Deutsche Forschungsgemeinschaft and the Alfried Krupp Stiftung (Dr. Brandt).

Received July 31, 1992. Accepted for publication in final form November 4, 1992.

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