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

Psychophysical data indicate that humans can discriminate visual scenes based on their skewness, i.e. the ratio of dark and bright patches within a visual scene. It has also been shown that at 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 suggesting that the underlying computation might 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 that the properties of the phototransduction cascade are universal across vertebrates, it is possible that 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 suggest the importance of non-linearity of the early photoreceptor for perception. Additionally, we found that stimulus skewness leads to a subtle change in photoreceptor kinetics. For negatively skewed stimuli, the impulse response functions of the cone peak later than for positively skewed stimuli. However, stimulus skewness does not affect the overall integration time of the cone. KEY POINTS: Humans can discriminate visual scenes based on skewness, i.e. the relative prevalence of bright and dark patches within a scene. Here, we show that 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 contrasts (bright patches). Unlike the implicit assumption often contained within models of downstream visual neurons, our data show that cone photoreceptors do not simply relay linearly filtered versions of visual stimuli to downstream circuitry, but that they also emphasize specific stimulus features. Given that the phototransduction cascade properties among vertebrate retinas are mostly universal, our data imply that the skew discrimination by human subjects reported in psychophysical studies might stem from the asymmetric gain function of the phototransduction cascade.