Nonlinear spatial integration underlies the diversity of retinal ganglion cell responses to natural stimuli

Abstract

How neurons encode natural stimuli is a fundamental question for sensory neuroscience. In the early visual system, standard encoding models assume that neurons linearly filter incoming stimuli through their receptive fields, but artificial stimuli, such as reversing gratings, often reveal nonlinear spatial processing. We investigated whether such nonlinear processing is relevant for the encoding of natural images in ganglion cells of the mouse retina. We found that standard linear receptive field models fail to capture the spiking activity for a large proportion of cells. These cells displayed pronounced sensitivity to fine spatial contrast, and local signal rectification was identified as the dominant nonlinearity. In addition, we also observed a class of nonlinear ganglion cells with opposite tuning for spatial contrast and a particular sensitivity for spatially homogeneous stimuli. Our work highlights receptive field nonlinearities as a crucial component for understanding early sensory encoding in the context of natural stimuli.