Enhancing the dark side: Asymmetric gain of cone photoreceptors underpins their discrimination of visual scenes based on their skewness.

KEY POINTS: Humans can discriminate visual scenes based on skewness – the relative prevalence of bright and dark patches within a scene. Here we show negatively skewed time-series stimuli induce larger responses in goldfish cone photoreceptors than comparable positively skewed stimuli. This response asymmetry originates from within the phototransduction cascade, where gain is higher for strong negative contrasts (dark patches) than for strong positive (bright patches) contrasts. Unlike the implicit assumption often contained within models of downstream visual neurons, our data shows cone photoreceptors do not simply relay linearly filtered versions of visual stimuli to downstream circuitry but instead they also emphasize specific stimulus features. As the phototransduction cascade properties among vertebrae retina are mostly universal, our data implies the skew discrimination by human subjects reported in psychophysical studies may stem from the phototransduction cascade’s asymmetric gain function.

ABSTRACT: Psychophysical data indicates humans can discriminate visual scenes based on their skewness – the ratio of dark and bright patches within a visual scene. It was also shown that on a phenomenological level this skew discrimination is described by the so-called Blackshot mechanism, which accentuates strong negative contrasts within a scene. Here we present a set of observations that suggest the underlying computation may start as early as the cone phototransduction cascade, whose gain is higher for strong negative contrasts than for strong positive contrasts. We recorded from goldfish cone photoreceptors and found that the asymmetry in the phototransduction gain leads to responses with larger amplitudes when using negatively, rather than positively, skewed light stimuli. This asymmetry in amplitude was present in the cone photocurrent, voltage response and synaptic output. Given the properties of the phototransduction cascade are universal across vertebrae, it is possible the mechanism shown here gives rise to a general ability to discriminate between scenes based only on their skewness, which psychophysical studies have shown humans can do. Thus, our data suggests the importance of the early photoreceptor non-linearity for perception. Additionally, we found that stimulus skewness leads to a subtle change in photoreceptor kinetics. For negatively skewed stimuli, the cone’s impulse response functions peak later than for positively skewed stimulus. However, stimulus skewness does not affect the cone’s overall integration time. This article is protected by copyright. All rights reserved.