Adaptive neural mechanism for listing's law revealed in patients with fourth nerve palsy

Abstract

Purpose: During fixation and saccades, human eye movements obey Listing's law, which specifies the eye's torsional angle as a function of its horizontal and vertical position. Torsion of the eye is in part controlled by the fourth nerve. This study investigates whether the brain adapts to defective torsional control after fourth nerve palsy.

Methods: Thirteen patients with fourth nerve palsy (11 chronic, 2 acute), and 10 normal subjects were studied with scleral search coils. With the head immobile, subjects made saccades to a target that moved between straight ahead and eight eccentric positions. At each target position, fixation was maintained for 3 seconds before the next saccade. From the eye position data, we computed the plane of best fit, referred to as Listing's plane. 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 paretic and nonparetic eyes in patients with chronic fourth nerve palsy obeyed Listing's law during fixation and saccades. However, Listing's planes in both eyes had abnormal orientations, being rotated temporally, meaning the eye excyclotorted during downgaze and incyclotorted during upgaze. In contrast, the paretic eye of patients with acute fourth nerve palsy violated Listing's law during saccades. During downward saccades, transient torsional deviations moved the paretic eye out of Listing's plane. Torsional drifts returned the paretic eye to Listing's plane during subsequent fixation.

Conclusions: During saccades, acute fourth nerve palsy violates Listing's law, whereas chronic palsy obeys it, indicating that neural adaptation can restore Listing's law by adjusting the innervations to the remaining extraocular muscles, even when one eye muscle remains paretic. The transient torsional deviations during downward saccades in acute palsy are attributed to pulse-step mismatch, as a result of lesions in the trochlear nerve that lead to an imbalance of phasic and tonic signals reaching the muscles.