Abnormal spatial localization with trigeminal-oculomotor synkinesis: Evidence for a proprioceptive effect

Summary: We examined spatial localization, using open-loop pointing to visual targets, in a patient with a congenital trigeminal-oculomotor synkinesis. This patient demonstrated abnormal co-activation of the left medial rectus muscle when the left lateral pterygoid contracted. Because one eye could be deviated in the absence of a normal oculomotor innervational command, the efference copy (derived from monitoring of central oculomotor commands) could be dissociated from the proprioceptive afferent signal (determined by the mechanical state of the extraocular muscles). Under conditions of monocular viewing with the normal right eye, when the covered left eye was adducted by the aberrant trigeminal innervation, the patient pointed to the left of the actual position of the target. This finding indicates that proprioceptive afference from the adducted, covered left eye was used in the process of spatial localization.While synkinetic adduction produced a shift in pointing in the opposite direction of rotation of the non-viewing eye, previous studies using passive deviation of the non-viewing eye in normal subjects reported a shift in pointing in the same direction as eye rotation (Gauthier et al., 1990; Bridgeman and Stark, 1991). We propose that this discrepancy is due to the different effects of passive eye rotation and active muscle contraction on the tendon organs of the extraocular muscles. On this basis, we hypothesize that the tendon organs, rather than the muscle spindles, are primarily responsible for the transduction of proprioceptive information about eye position in the orbit.