9How neurons encode natural stimuli is a fundamental question for sensory neuroscience. In the early 10 visual system, standard encoding models assume that neurons linearly filter incoming stimuli through 11 their receptive fields, but artificial stimuli, such as reversing gratings, often reveal nonlinear spatial 12 processing. We investigated whether such nonlinear processing is relevant for the encoding of natural 13 images in ganglion cells of the mouse retina. We found that standard linear receptive field models fail 14 to capture the spiking activity for a large proportion of cells. These cells displayed pronounced 15 sensitivity to fine spatial contrast, and local signal rectification was identified as the dominant 16nonlinearity. In addition, we also observed a class of nonlinear ganglion cells with opposite tuning for 17 spatial contrast and a particular sensitivity for spatially homogeneous stimuli. Our work highlights 18 receptive field nonlinearities as a crucial component for understanding early sensory encoding in the 19 context of natural stimuli. 20 2007). Furthermore, linear RF models fail to predict responses of some ganglion cells to finely 40 structured white-noise stimulation (Freeman et al., 2015;Liu et al., 2017). Such failures are linked to 41 the nonlinear integration of excitatory signals in the RF center, which originate from presynaptic 42 bipolar cells (Borghuis et al., 2013;Demb et al., 2001a;Turner and Rieke, 2016). 43This raises the question to what extent nonlinear encoding plays a role in natural vision. In terms of 44 spatial structure, natural stimuli lie in between finely detailed and coarse stimuli, because the light 45 intensities of nearby regions in natural images are correlated (Burton and Moorhead, 1987), yet object 46 boundaries can lead to edges and strong changes of stimulus intensity over short distances (Turiel and 47 salamander retina (Liu et al., 2017;McIntosh et al., 2017) and that their performance is cell-type 55 specific (Turner and Rieke, 2016). 56In this work, we establish a connection of spatial RF nonlinearities to natural stimulus encoding in 57 retinal ganglion cells. We do so in the mouse retina, in which spatial integrationas measured with 58artificial stimuliappears to display a broad scope (Carcieri et al., 2003), with spatially linear 59 (Johnson et al., 2018;Krieger et al., 2017) as well as strongly nonlinear cells (Jacoby and Schwartz, 60 2017;Mani and Schwartz, 2017; Zhang et al., 2012). We first show that linear RF models 61 successfully predict responses to natural images for some ganglion cells and substantially fail for 62 others. We then connect model failure to spatial nonlinearities in the RF center. Finally, we analyze 63 the spatial integration characteristics of specific functional cell types, showing that cells of the same 64 type have similar properties. 65
Results
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Performance of linear-nonlinear models for predicting responses to natural images varies 67 strongly among retinal ganglion cells 68In order to survey whether linear...