Development of the kitten visual cortex depends on the relationship between the plane of eye movements and visual inputs.

1. Previous experiments have demonstrated that eye movements, acting through the extraocular muscle (EOM) proprioceptive afferents, are necessary for the development of orientation selectivity in the cells of the kitten visual cortex. New experiments were carried out to study the effect of the plane of eye movements on the preferred orientation acquired by the visual cortical cells. 2. Dark-reared (DR) kittens were operated on at 5-6 weeks of age. In the first series of experiments, 4 out of the 6 EOMs were removed bilaterally in such a way that both eyes could only move in a single plane, either vertical or horizontal. In the second series of experiments, the same operation was performed on one eye which was also sutured shut and, on the other side, the EOM were deafferented by intracranial section of the ophthalmic branch of Vth nerve and the eye left open. 3. 1-4 days after surgery the kittens were given 6 h of visual experience and 12 h later were prepared for visual cell recording in Area 17. 4. In kittens of the first series: orientation selectivity developed in the majority (60-65%) of visual cells, most of which encoded horizontal orientations when the eyes had moved in the vertical plane and vertical orientations when the eyes had moved in the horizontal plane. These results show that the plane of eye movements during early visual experience influences the distribution of preferred orientations with an orthogonal relation. Ocular dominance histograms were "strabismic like". 5. In kittens of the second series: orientation selectivity developed in 40-50% of cells, about half of which were tuned for the orientation orthogonal to the direction of movement of the occluded eye, as in experiment I. The seeing, deafferented eye, presumably would have sent normal visual inputs centrally, corresponding to displacements on the retina in every direction since the ocular motility of that eye had not been disturbed. However, proprioceptive information about its movements was suppressed. As only some of the EOMs of the occluded eye were still present and connected, the conclusion is that the observed influence of the plane of eye movements acts through the proprioceptive afferents.(ABSTRACT TRUNCATED AT 400 WORDS)