The first interneuron of the mouse visual system is tailored to the natural environment through morphology and electrical coupling

Abstract

The topographic complexity of the mouse retina has long been underestimated, as obvious specializations, like a fovea or visual streak, are absent. However, anatomical and functional gradients exist. It was recently shown that receptive fields of retinal ganglion cells change their shape along the dorso-ventral retinal axis. These variations likely reflect the non-uniform statistics of the visual environment which vary dramatically from ground to sky. Horizontal cells are the first visual interneurons and dictate the synaptic signaling between photoreceptors and bipolar cells by lateral interactions, thereby shaping the receptive fields of down-stream neurons. Thus, we asked whether regional specializations are present at this earliest stage of synaptic circuitry, i.e. at the level of horizontal cells. We analyzed horizontal cell density distributions, morphological properties, localization of gap junction proteins, and the spatial extent of horizontal cell electrical coupling across complete retinas. All of these horizontal cell key features were asymmetrically organized along the dorso-ventral axis. Dorsal horizontal cells were less densely distributed, had larger dendritic trees, and electrical coupling was more extensive than in their ventral counterparts. The steepest change along this gradient occurred at the opsin transition zone of photoreceptors, i.e. the mouse visual horizon. Therefore, our results show that the cellular and synaptic organization of the mouse visual system are adapted to the visual environment at the earliest possible level, and that horizontal cells are well suited to form the cellular substrate for the global gradient previously described for the receptive field structures of retinal ganglion cells.