Effects of eye and neck muscle proprioception on ocular motor control in normal and strabismic subjects

Abundant proprioceptive information originates in eye and neck muscles but their role in normal visual function is unknown. Under experimental conditions, proprioceptive activation induces illusory visual movement, whereas clinical evidence indicates that proprioceptive dysfunction causes disturbances in spatial orientation. Animal experiments have shown that proprioceptive disturbance impede normal development of binocular function.

The present investigations examined the consequences of proprioceptive activation of eye and neck muscles on gaze direction, space localization and control of accommodative vergence movements. These studies included patients with disturbances of binocularity due to intermittent and manifest strabismus together with subjects with normal binocular vision.

Changes in eye position induced by vibration of eye muscle were recorded with an infrared system in 11 normal and 10 exotropic subjects. Lateral rectus vibration induced a temporally directed (abductive) eye position change in normal subjects, but a nasally directed (adductive) eye position change in exotropics. These data suggest that signals from eye muscle proprioceptors are processed differently in normals and strabismics.

Eye position changes induced by neck muscle vibration were studied in 8 normal and 23 strabismic subjects. These experiments showed that the direction of eye position changes were the same in normals and intermittent exotropics with good binocular function. However in subjects with manifest strabismus and poor binocular function, vibration of lateral rotating muscles of the neck resulted in eye position changes that differed from normals. These data indicate that proprioceptive information derived from the neck muscles are involved in directing gaze. However, differences in horizontal gaze control exist between normal and strabismic subjects which may be related to differences in the state of binocular vision.

The effects of eye and neck muscle vibration on visual target localization was studied in 11 normal and 17 strabismic subjects. In all stimulation conditions, the direction of the pointing shifts were the same in normals and the intermittent exotropic patient with good binocular vision. However, the shift in pointing direction that occurred as a result of horizontal muscle stimulation differed between normal subjects and those with manifest strabismus and poor binocular vision. These differences are probably related to the state of binocular functions.

Control experiments showed that no artifacts occurred due to head movements or extra visual or extra-proprioceptive stimulation. Together these studies show that spatial orientation and the control of target position involve an interaction of proprioceptive feedback from eye and neck muscles together with information from the visual system. Binocular dysfunction in strabismus is associated with deficiencies in lateral target positioning.

The dynamics of accommodative vergence movements induced by monocular viewing were investigated. The amplitude of the accommodative vergence movements was highest during the non-dominant eye viewing at a particular stimulus intensity. Accommodative vergence angles varied depending on the leading eye which drove the accommodative vergence system.

The role of neck muscle proprioception on the dynamics of accommodative vergence movements was studied in normals. When the non-dominant eye was fixated on the target, stimulation of the neck muscles shortened the time constant of the accommodative vergence movement in the covered eye. These data demonstrate that extraretinal signals from neck proprioception influence not only static eye position, but also the dynamics of monocularly driven accommodative vergence movements when the non-dominant eye was the viewing eye.