Induced extraocular muscle afferent signals: from pigeons to people

While the muscles that move the eyes, the extraocular muscles (EOM), are well endowed with proprioceptors, afferent signals from these receptors are usually assumed to play little or no role in the control of eye movement. In a series of experiments, a suction contact lens was used to impose movements on one eye, thus inducing afferent signals. Single unit activity was recorded centrally (to examine the interactions between EOM afferent signals and visual or vestibular signals), or the movements of the other eye were measured (to investigate their effects on the output of the oculomotor system). In a model preparation, the decerebrate pigeon, EOM afferent signals modified single unit activity in the medial vestibular nucleus, and the third and sixth motor nuclei, during sinusoidal vestibular stimulation. When one eye was moved to mimic the vestibulo-ocular reflex (VOR), movement faster than required for compensation for a given head velocity reduced the gain of single unit vestibular responses. In awake, alert pigeons the overall output of the VOR, as evidenced by movements of the other eye, was modified. In humans, when one eye was impeded, the saccades and smooth pursuit executed by the other eye were altered. Taken together, these results suggest that EOM afferent signals play a functional role in the shaping of eye movement.