Effects of phase correlations in naturalistic stimuli on quantitative information coding by fly photoreceptors

Natural visual scenes are rarely random. Instead, intensity and wavelength change slowly in time and space over many regions of the scene, so that neighboring temporal and spatial visual inputs are more correlated and contain less information than truly random signals. It has been suggested that sensory optimization to match these higher order correlations (HOC) occurs at the earliest visual stages, and that photoreceptors can process temporal natural signals more efficiently than random signals. We tested this early-stage hypothesis by comparing the information content of Calliphora vicina photoreceptor responses to naturalistic inputs before and after removing HOC by randomizing phase. Forty different, 60-s long, naturalistic sequences (NS) were used, together with randomized-phase versions of the same sequences to give pink noise (PN) so that each input pair had identical means, variances, mean contrasts, and power spectra. We measured the information content of inputs and membrane potential responses by three different methods: coherence, mutual information, and compression entropy. We also used entropy and phase statistics of each pair as measures of HOC. Responses to randomized signals generally had higher gain, signal-to-noise ratio, and information rates than responses to NS. Information rate increased with a strong, positive, linear correlation to phase randomization within sequence pairs. This was confirmed by varying the degree of phase randomization. Our data indicate that individual photoreceptors encode input information by Weber's law, with HOC within natural sequences reducing information transfer by decreasing the number of local contrast events that exceed the noise-imposed threshold. NEW & NOTEWORTHY Natural visual scenes feature statistical regularities, or higher order correlations (HOC), both in time and space, to encode surfaces, textures, and object boundaries. Visual systems rely on this information; however, it remains controversial whether individual photoreceptors can discriminate and enhance information encoded in HOC. Here we show that the more HOC the stimulus contains, the lower the information transfer rate of photoreceptors. We explain our findings by applying the Weber's paradigm of differential signal perception.