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Adaptive Neural Mechanism for Listing’s Law Revealed in Patients with Skew Deviation Caused by Brainstem or Cerebellar Lesion

¹From the Departments of Physiology and ²Ophthalmology and Vision Science, and the ³Division of Neurology, University Health Network, and the Hospital for Sick Children, University of Toronto, Toronto, Ontario, Canada.

PURPOSE. Skew deviation is a vertical strabismus caused by damage to the otolithic–ocular reflex pathway and is associated with abnormal ocular torsion. This study was conducted to determine whether patients with skew deviation show the normal pattern of three-dimensional eye control called Listing’s law, which specifies the eye’s torsional angle as a function of its horizontal and vertical position.

METHODS. Ten patients with skew deviation caused by brain stem or cerebellar lesions and nine normal control subjects were studied. Patients with diplopia and neurologic symptoms less than 1 month in duration were designated as acute (n = 4) and those with longer duration were classified as chronic (n = 10). Serial recordings were made in the four patients with acute skew deviation. With the head immobile, subjects made saccades to a target that moved between straight ahead and eight eccentric positions, while wearing search coils. At each target position, fixation was maintained for 3 seconds before the next saccade. From the eye position data, the plane of best fit, referred to as Listing’s plane, was fitted. Violations of Listing’s law were quantified by computing the "thickness" of this plane, defined as the SD of the distances to the plane from the data points.

RESULTS. Both the hypertropic and hypotropic eyes in patients with acute skew deviation violated Listing’s and Donders’ laws—that is, the eyes did not show one consistent angle of torsion in any given gaze direction, but rather an abnormally wide range of torsional angles. In contrast, each eye in patients with chronic skew deviation obeyed the laws. However, in chronic skew deviation, Listing’s planes in both eyes had abnormal orientations.

CONCLUSIONS. Patients with acute skew deviation violated Listing’s law, whereas those with chronic skew deviation obeyed it, indicating that despite brain lesions, neural adaptation can restore Listing’s law so that the neural linkage between horizontal, vertical, and torsional eye position remains intact. Violation of Listing’s and Donders’ laws during fixation arises primarily from torsional drifts, indicating that patients with acute skew deviation have unstable torsional gaze holding that is independent of their horizontal–vertical eye positions.