Simple Model for Encoding Natural Images by Retinal Ganglion Cells with Nonlinear Spatial Integration

Abstract

AbstractA central goal in sensory neuroscience is to understand the neuronal signal processing involved in the encoding of natural stimuli. A critical step towards this goal is the development of successful computational encoding models. For ganglion cells in the vertebrate retina, the development of satisfactory models for responses to natural visual scenes is an ongoing challenge. Standard models typically apply linear integration of visual stimuli over space, yet many ganglion cells are known to show nonlinear spatial integration, in particular when stimulated with contrast-reversing gratings. We here study the influence of spatial nonlinearities in the encoding of natural images by ganglion cells, using multielectrode-array recordings from isolated salamander and mouse retinas. We assess how responses to natural images depend on first- and second-order statistics of spatial patterns inside the receptive field. This leads us to a simple extension of current standard ganglion cell models. We show that taking not only the weighted average of light intensity inside the receptive field into account but also its variance over space can partly account for nonlinear integration and substantially improve response predictions of responses to novel images. We find that response predictions for salamander ganglion cell classes with large receptive fields profit most from including spatial contrast information. Finally, we demonstrate how this model framework can be used to assess the spatial scale of nonlinear integration. Our results underscore that nonlinear spatial stimulus integration in the salamander retina translates to stimulation with natural images. Furthermore, the introduced model framework provides a simple, yet powerful extension of standard models and may serve as a benchmark for the development of more detailed models of the nonlinear structure of receptive fields.Author SummaryFor understanding how sensory systems operate in the natural environment, an important goal is to develop models that capture neuronal responses to natural stimuli. For retinal ganglion cells, which connect the eye to the brain, current standard models often fail to capture responses to natural visual scenes. This shortcoming is at least partly rooted in the fact that ganglion cells may combine visual signals over space in a nonlinear fashion. We here show that a simple model, which not only considers the average light intensity inside a cell’s receptive field but also the variance of light intensity over space, can partly account for these nonlinearities and thereby improve current standard models. This provides an easy-to-obtain benchmark for modeling ganglion cell responses to natural images.