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

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 demonstrate that the underlying computation starts 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 higher amplitude of the responses to negatively than to positively skewed light stimuli. This asymmetry in the amplitude was present in the photocurrent, voltage response and cone synaptic output. These results highlight 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 cones impulse response functions peak later than for positively skewed stimulus. However, stimulus skewness does not affect the cones overall integration time.