Anatomical origins of ocular dominance in mouse primary visual cortex

Abstract

Ocular dominance (OD) plasticity is a classic paradigm for studying the effect of experience and deprivation on cortical development, and is manifested as shifts in the relative strength of binocular inputs to primary visual cortex (V1). The mouse has become an increasingly popular model for mechanistic studies of OD plasticity and, consequently, it is important that we understand how binocularity is constructed in this species. One puzzling feature of the mouse visual system is the gross disparity between the physiological strength of each eye in V1 and their anatomical representation in the projection from retina to the dorsal lateral geniculate nucleus (dLGN). While the contralateral-to-ipsilateral (C/I) ratio of visually evoked responses in binocular V1 is ∼2:1, the ipsilateral retinal projection is weakly represented in terms of retinal ganglion cell (RGC) density where the C/I ratio is ∼9:1. The structural basis for this relative amplification of ipsilateral eye responses between retina and V1 is not known. Here we employed neuroanatomical tracing and morphometric techniques to quantify the relative magnitude of each eye's input to and output from the binocular segment of dLGN. Our data are consistent with the previous suggestion that a point in space viewed by both eyes will activate 9 times as many RGCs in the contralateral retina as in the ipsilateral retina. Nonetheless, the volume of the dLGN binocular segment occupied by contralateral retinogeniculate inputs is only 2.4 times larger than the volume occupied by ipsilateral retinogeniculate inputs and recipient relay cells are evenly distributed among the input layers. The results from our morphometric analyses show that this reduction in input volume can be accounted for by a three-to-one convergence of contralateral eye RGC inputs to dLGN neurons. Together, our findings establish that the relative density of feed-forward dLGN inputs determines the C/I response ratio of mouse binocular V1.