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

Abstract

1. 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 inter-stimulus intervals, were studied in chloralose-anaesthetized cats. 2. Most units responded to visual stimuli and about half also gave phasic excitatory responses to stretch of e.o.m. 3. Signals from the e.o.m. of each eye reach both superior colliculi; only those in the colliculus ipsilateral to the e.o.m. stretched were studied in detail. 4. A variety of control experiments provided evidence that the signal leading to the responses to e.o.m. stretch was extraretinal. The strong probability is that the receptors responsible were in the extrinsic ocular muscles or their tendons. 5. Of fifty-six units, twenty-four (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 had been destroyed. 6. Interactions were found with both stationary and moving visual stimuli. They involved either enhancement or reduction (sometimes abolition) of the response to either e.o.m. or visual stimulation, particularly the latter. 7. Units with interactions showed one of three types of behaviour. (1) Excitatory responses to visual and e.o.m. stimuli given singly, and interactions when the two types of stimulus were paired at some time intervals. Suppression and abolition of visual responses by preceding e.o.m. stretch was common. (2) Units with little or no excitatory response to e.o.m. stretch applied alone, but with showed reduction of their visual responses by preceding e.o.m. stretch. (3) Units with minimal responses to either type of stimulus presented alone but which gave markedly enhanced responses when visual and e.o.m. stimuli were paired. 8. These interactions between proprioceptive and retinal signals are thought to allow retinal image movements which result from saccades to be distinguished from those due to movement of objects in the external world.