Afferent signals from pigeon extraocular muscles modify the activity of neck muscles during the vestibulocollic reflex.

Movements of the head and eye which, together, result in changes in the direction of gaze are linked in a number of species, including man, and eye position is known to affect the activity of neck muscles. This head-eye linkage has generally been ascribed to modification of neck muscle activity by internal estimates of eye position derived from motor commands. We have recently shown that afferent signals from stretch receptors in the extraocular muscles are involved in the moment-to-moment control of eye movements during the vestibuloocular reflex (VOR). We have now studied the interactions between head and eye movements by recording the electromyographic activity of several neck muscles during horizontal (yaw) or frontal (roll tilt) vestibular stimulation. Such a stimulus evokes a VOR in the eyes and a vestibulocollic reflex (VCR) in neck muscles. Imposing movements on one eye at saccadic velocities produced considerable inhibition of the VCR response of a number of neck muscles. The magnitude of these effects was dependent on the parameters of the imposed eye movement. Thus systematic changes were seen when the amplitude, velocity or direction of eye movement was varied. Movement of the eye in the opposite direction to that produced by a normal VOR produced a large inhibition of the VCR response, whereas movements in the same direction as the VOR produced only modest inhibition of the VCR response of the neck muscles tested. Slow, sinusoidal, imposed eye movements that mimicked the slow phase of the VOR produced changes in the gain of the VCR response which appear to correct for errors in the imposed eye velocity and thus tend to maintain the direction of gaze. The results show that changes in eye position have striking effects on the electromyographic activity of neck muscles during the VCR, and strongly suggest that extraocular muscle afferent signals are involved in head-eye coordination.