Variations in photoreceptor throughput to mouse visual cortex and the unique effects on tuning

Visual input to primary visual cortex (V1) depends on highly adaptive filtering in the retina. In turn, isolation of V1 computations requires experimental control of retinal adaptation to infer its spatio-temporal-chromatic output. Here, we measure the balance of input to mouse V1, in the anesthetized setup, from the three main photoreceptor opsins—M-opsin, S-opsin, and rhodopsin—as a function of two stimulus dimensions. The first dimension is the level of light adaptation within the mesopic range, which governs the balance of rod and cone inputs to cortex. The second stimulus dimension is retinotopic position, which governs the balance of S- and M-cone opsin input due to the opsin expression gradient in the retina. The fitted model predicts opsin input under arbitrary lighting environments, which provides a much-needed handle on in-vivo studies of the mouse visual system. We use it here to reveal that V1 is rod-mediated in common laboratory settings yet cone-mediated in natural daylight. Next, we compare functional properties of V1 under rod and cone-mediated inputs. The results show that cone-mediated V1 responds to 2.5-fold higher temporal frequencies than rod-mediated V1. Furthermore, cone-mediated V1 has smaller receptive fields, yet similar spatial frequency tuning. V1 responses in rod-deficient (Gnat1(−/−)) mice confirm that the effects are due to differences in photoreceptor opsin contribution.