Receptive-field properties and neuronal connectivity in striate and parastriate cortex of contour-deprived cats

Abstract

An attempt was made to relate the alterations of cortical receptive fields as they result from binocular visual deprivation to changes in afferent, intrinsic, and efferent connections of the striate and parastriate cortex. The experiments were performed in cats aged at least 1 jr with their eyelids sutured closed from birth. The results of the receptive-field analysis in A17 confirmed the reduction of light-responsive cells, the occasional incongruity of receptive-field properties in the two eyes, and to some extent also the loss of orientation and direction selectivity as reported previously. Other properties common to numerous deprived receptive fields were the lack of sharp inhibitory sidebands and the sometimes exceedingly large size of the receptive fields. Qualitatively as well as quantitatively, similar alterations were observed in area 18. A rather high percentage of cells in both areas had, however, preserved at least some orientation preference, and a few receptive fields had tuning properties comparable to those in normal cats. The ability of area 18 cells in normal cats to respond to much higher stimulus velocities than area 17 cells was not influenced by deprivation. The results obtained with electrical stimulation suggest two main deprivation effects: 1) A marked decrease in the safety factor of retinothalamic and thalamocortical transmission. 2) A clear decrease in efficiency of intracortical inhibition. But the electrical stimulation data also show that none of the basic principles of afferent, intrinsic, and efferent connectivity is lost or changed by deprivation. The conduction velocities in the subcortical afferents and the differentiation of the afferents to areas 17 and 18 into slow- and fast-conducting projection systems remain unaltered. Intrinsic excitatory connections remain functional; this is also true for the disynaptic inhibitory pathways activated preferentially by the fast-conducting thalamocortical projection. The laminar distribution of cells with monosynaptic versus polsynaptic excitatory connections is similar to that in normal cats. Neurons with corticofugal axons remain functionally connected and show the same connectivity pattern as those in normal cats. The nonspecific activation system from the mesencephalic reticular formation also remains functioning both at the thalamic and the cortical level. We conclude from these and several other observations that most, if not all, afferent, intrinsic, and efferent connections of areas 17 and 18 are specified from birth and depend only little on visual experience. This predetermined structural plan, however, allows for some freedom in the domain of orientation tuning, binocular correspondence, and retinotopy which is specified only when visual experience is possible.