Interactions between extraocular proprioceptive and visual signals in the superior colliculus of the cat.

Abstract

The responses of units in the superficial layers of the superior colliculus to stretch of extrinsic ocular muscles (e.o.m.) and to visual stimuli, delivered singly and paired at various interstimulus intervals, were studied in chloralose-anesthetized cats. Most units responded to visual stimuli and about half gave phasic excitatory responses to stretch of e.o.m. Signals from the e.o.m. of each eye reach both superior colliculi; only those in the colliculus ipsilateral to the stretched e.o.m. were studied in detail. A variety of control experiments indicated the signal leading to the responses to e.o.m. stretch was extraretinal. The receptors responsible were probably in the extrinsic ocular muscles or their tendons. Of 56 units, 24 (43%) showed definite interactions between the effects of visual stimuli delivered to the left eye and those due to stretch of e.o.m. of the right eye whose retina was destroyed. Interactions were found with stationary and moving visual stimuli. They involved enhancement or reduction (sometimes abolition) of the response to e.o.m. or visual stimulation, particularly the latter. Units with interactions showed 1 of 3 types of behavior: excitatory responses to visual and e.o.m. stimuli given singly and interactions when the 2 types of stimulus were paired at some time intervals. Suppression and abolition of visual responses by preceding e.o.m. stretch was common. Some units with little or no excitatory response to e.o.m. stretch applied alone showed reduction of their visual responses by preceding e.o.m. stretch. Other units with minimal responses to either type of stimulus presented alone gave markedly enhanced responses when visual and e.o.m. stimuli were paired. These interactions between proprioceptive and retinal signals apparently allow retinal image movements resulting from saccades as distinguished from those due to movement of objects in the external world.