Feedback from V1 and inhibition from beyond the classical receptive field modulates the responses of neurons in the primate lateral geniculate nucleus

Abstract

It is well established that the responses of neurons in the lateral geniculate nucleus (LGN) can be modulated by feedback from visual cortex, but it is still unclear how cortico-geniculate afferents regulate the flow of visual information to the cortex in the primate. Here we report the effects, on the gain of LGN neurons, of differentially stimulating the extraclassical receptive field, with feedback from the striate cortex intact or inactivated in the marmoset monkey, Callithrix jacchus. A horizontally oriented grating of optimal size, spatial frequency, and temporal frequency was presented to the classical receptive field. The grating varied in contrast (range: 0–1) from trial to trial, and was presented alone, or surrounded by a grating of the same or orthogonal orientation, contained within either a larger annular field, or flanks oriented either horizontally or vertically. V1 was ablated to inactivate cortico-geniculate feedback. The maximum firing rate of LGN neurons was greater with V1 intact, but was reduced by visually stimulating beyond the classical receptive field. Large horizontal or vertical annular gratings were most effective in reducing the maximum firing rate of LGN neurons. Magnocellular neurons were most susceptible to this inhibition from beyond the classical receptive field. Extraclassical inhibition was less effective with V1 ablated. We conclude that inhibition from beyond the classical receptive field reduces the excitatory influence of V1 in the LGN. The net balance between cortico-geniculate excitation and inhibition from beyond the classical receptive field is one mechanism by which signals relayed from the retina to V1 are controlled.