Proprioceptive signals from extraocular muscles gate experience-dependent modifications of receptive fields in the kitten visual cortex

The abolition of proprioceptive signals from extraocular muscles impedes the experience dependent development of normal cortical receptive fields and prevents the vision dependent reorganization of binocular connectivity such as occurs in strabismic and monocularly deprived kittens.

Abstract

We examined to what extent the proprioceptive signals from extraocular muscles control the vision dependent development of striate cortex functions. In six dark-reared, four-week old kittens we severed the ophthalmic branches of the Vth cranial nerves bilaterally in order to interrupt the proprioceptive afferent input from extraocular muscles. In addition, in order to induce experience-dependent modifications of binocularity we made three of the kittens strabismic by unilateral section of the rectus lateralis muscle and monocularly deprived the three other kittens by lid suture. After these interventions all kittens were raised on a normal day/night schedule. Eight weeks (n = 5) and one year (n = 1) after surgery we examined the receptive field properties of striate cortex neurons with single cell recording. In the strabismic and monocularly deprived kittens 81% and 73%, respectively, of the responsive cells had remained binocular. The ocular dominance distribution in the monocularly deprived kittens was biased only moderately towards the open eye. In both preparations a large fraction of the cells responded sluggishly to optimally aligned light stimuli and had abnormally low orientation selectivity. The few cells (about 20% in both preparations) with normal orientation selectivity responded also vigorously to light. Most of these cells had simple receptive fields and were monocular. The ocular dominance distribution of these mature cells was strongly biased towards the open eye in the monocularly deprived kittens and it was U-shaped in the strabismic kittens. In both preparations the orientation preferences of these mature cells were strongly biased towards vertical and horizontal. We conclude from these results that the abolition of proprioceptive signals from extraocular muscles impedes the experience dependent development of normal cortical receptive fields and prevents the vision dependent reorganization of binocular connectivity such as occurs in strabismic and monocularly deprived kittens. We propose that the control of cortical development by non-retinal, proprioceptive signals is indispensable if the vision dependent modifications of cortical connectivity serve to optimize binocular correspondence.