Synaptic Physiology and Receptive Field Structure in the Early Visual Pathway of the Cat

How does the cortical circuitry analyze the visual scene? Here we explore the earliest levels of striate cortical processing: the first stage, where orientation sensitivity emerges, and the second stage, where stimulus selectivity is further refined. The approach is wholecell recording from cat in vivo. Neurons in the lateral geniculate nucleus of the thalamus have circular receptive fields whose subregions, center and surround are concentrically arranged and have the reverse sign, on or off. These neurons supply cortical simple cells, whose receptive fields have on and off subregions that are elongated and lie side by side. Feedforward models hold that orientation sensitivity depends on this thalamocortical change in receptive field structure and an arrangement within subregions such that stimuli of the reverse contrast evoke synaptic responses of the opposite polarity-push-pull. Our work provides support for feedforward models and emphasizes that push-pull is key in the geniculostriate pathway, preserved from retina by thalamic relay cells and reiterated, point by point, by cortical simple cells. Also, we help define the cortical push-pull circuit by identifying inhibitory simple cells. Lastly, separate experiments that compare the first and second levels of cortical processing suggest that differences in the synaptic physiology of connections at the two (thalamocortical versus intracortical) stages underlie differential selectivity for properties such as motion.