Ocular muscle proprioception and visual localization of targets in man

Passive deviation of one eye through 18 degrees, 30 degrees and 42 degrees, achieved by force applied to a sucked-on contact lens, caused the direction of visual targets seen by the other eye to be misjudged in the direction of the passive movement by an amount roughly one-sixth of the angle of passive deviation. The result was the same when the perceived direction was indicated by hand, as when the instant at which a moving target seemed straight ahead was signalled. This result is interpreted by considering that muscular efferents were identical in normal and eye-deviated subjects. The main difference between the two target localization conditions results from the proprioceptor output of the deviated eye. Our data demonstrate that the assessment of the direction of a target seen by an eye that is free to move depends in part on information received by the brain from proprioceptors in the orbit (in our case the contralateral orbit). It would be surprising if the ipsilateral orbit did not contribute as much or more. We therefore consider that this constitutes clear evidence against the pure outflow theory of visual direction judgement (Helmholz, 1867), additional to that provided by the all-or-nothing situation of complete versus incomplete oculomotor paralysis. Two models have previously been proposed to describe the function of the visual localization mechanism. Both assume that the necessary information is derived from the coding of the position of the eye in the orbit, either through a copy of the muscular activation or through eye muscle proprioception. We propose an alternative model in which both afferent and efferent signals from all actively contracted or stretched muscles provide the necessary information to the CNS. The data gathered so far from normal subjects made strabismic with a suction lens, and from a fair proportion of strabismic patients, support our model describing the mechanism of localization of a single punctate target in darkness.