Abstract

SummaryNeurons in sensory systems are often tuned to particular stimulus features. During complex naturalistic stimulation, however, multiple features may simultaneously affect neuronal responses, which complicates the readout of individual features. To investigate feature representation under complex stimulation, we studied how direction-selective ganglion cells in salamander retina respond to texture motion where direction, velocity, and spatial pattern inside the receptive field continuously change. We found that the cells preserve their direction preference under this stimulation, yet their direction encoding becomes ambiguous due to simultaneous activation by luminance changes. The ambiguities can be resolved by considering populations of direction-selective cells with different preferred directions. This gives rise to synergistic motion decoding, yielding more information from the population than the summed information from single-cell responses. Strong positive response correlations between cells with different preferred directions amplify this synergy. Our results show how correlated population activity can enhance feature extraction in complex visual scenes.

Highlights

  • A central finding for many sensory systems is that neurons are tuned to specific stimulus features, such as orientation and motion direction of visual stimuli, or pitch and spatial direction of an acoustic sound

  • We recorded the activity of many ganglion cells simultaneously from isolated salamander retina with multielectrode arrays and identified direction-selective cells based on their responses to drifting gratings (Figure 1A)

  • Given that our goal here is to analyze the encoding of texture motion, we focused our analysis on the type that responds well under global motion

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Summary

Introduction

A central finding for many sensory systems is that neurons are tuned to specific stimulus features, such as orientation and motion direction of visual stimuli, or pitch and spatial direction of an acoustic sound. For example, direction-selective ganglion cells respond with increased activity to visual stimulus motion in a specific direction but are suppressed by motion in the opposite direction (Barlow and Hill, 1963; Borst and Euler, 2011; Lettvin et al, 1959; Mauss et al, 2017; Wei, 2018) This direction tuning is thought to support the tracking of retinal slip and the stabilization of gaze position (Sabbah et al, 2017; Yonehara et al, 2016) as well as the detection of moving objects (Marques et al, 2018; Vaney et al, 2001). Direction-selective neurons in the visual system, for example, are traditionally studied with uniformly moving gratings or spots of light, where the direction of motion is varied to characterize the neurons’ directional tuning

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