Vertical eye position control in darkness: orbital position and body orientation interact to modulate drift velocity

How stable is vertical eye-in-head position control in darkness when no visual targets are present? We evaluated this while varying both body-in-space orientation and eye-in-orbit position in six subjects who were free from oculomotor/vestibular disease. Vertical eye movements were monitored using a CCD-video tracking system, and results were confirmed on one subject with the magnetic search coil. Three body orientations were used: (1) seated upright; (2) supine; and (3) prone. In each of these body orientations starting eye-in-orbit position was varied in quasi-random order from -20 to +20 deg, while vertical eye drift was monitored for a 90 sec period at each position. Subjects were instructed to hold their eyes as steady as possible. The relationship between body orientation/eye position and vertical eye drift velocity was examined using a linear regression technique. In contrast to prior clinical reports, normals exhibit a vertical nystagmus/drift in darkness. Moreover, slow-phase eye velocity was found to be dependent on eye-in-orbit position in the upright and supine body orientations. This pattern of eye drift mirrors Alexander's Law, with significantly increased drift velocities when subjects looked in the direction of their re-centering saccades (P < 0.05 or better). Body-in-space orientation also modulated the eye drift velocity, with significant differences in rate of eye drift (P < 0.05 or better) between extremes of body orientation (supine and prone) for five out of six subjects. The stability of the vertical oculomotor control system in the absence of visual input is strongly affected by body-in-space orientation and eye-in-orbit position: manipulating either of these variables results in non-random patterns of drift. These results are discussed using a multiple-input model of vertical eye-in-head position control.