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

Abstract

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.

Speed of phototransduction in the microvillus regulates the accuracy and bandwidth of the rhabdomeric photoreceptor

“…Importantly, while the overall noise decreased as a function of 1= ffi ffi ffi n p , SNR even at the high summation level of 100 QBs did not exceed 10 when all sources of transduction noise and the photon noise were present ( Figs 10G and 11С). This is consistent with the data from P. americana [28] and blow fly [33]. In order to improve SNR further by 10-fold, the number of QBs in the impulse response should increase by 100-fold, to the very high level of 10,000.…”

“…The study investigated introduction of noise at two signal processing stages: from a stimulus sequence to the actual absorbed photon sequence and then from the latter to the QB sequence. Essentially, this approach, although based on the minimum mean squared error distortion function, resembles that for determining information rate from coherence between input and output using a cross-correlation function [ 33 ]. The time delay term that emerges in both approaches as an information-destroying factor represents a well-known problem [ 34 ].…”

“…This is consistent with the data from P . americana [ 28 ] and blow fly [ 33 ]. In order to improve SNR further by 10-fold, the number of QBs in the impulse response should increase by 100-fold, to the very high level of 10,000.…”

A simple method for generating arbitrary Gaussian noise and compensating filter properties of a stimulator to measure the frequency response function of a mechanosensory sensillum

“…2). Dependence of TF on stimulus properties has also been shown, for example, in y photoreceptors using natural-like, GWN, or random Gaussian stimuli with the same amplitude spectrum as the natural stimuli (Song and Juusola 2014; Ignatova et al 2018). In primary sensory cells, such as the sensory cell of a liform sensillum, stimulus encoding is highly nonlinear because of the action potential threshold, phase-locking, recti cation, and response amplitude saturation (French 2009;French and Pfeiffer 2018).…”

Changes in electrophysiological properties of photoreceptors in Periplaneta americana associated with the loss of screening pigment

“…Increased signal gain in W-E photoreceptors is probably caused by improved effective illumination of the photoreceptor by stray light, which under these experimental conditions does not add noise. However, visual stimulation arriving from an actual natural scene, while changing from point to point in space, is partly spatially correlated (Ignatova et al 2018). Thus, stray light produced by summation across the retina would not be constant but partly contrast-modulated and probably out of phase with the light propagating along the optical axis of the ommatidium.…”