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

Abstract

Phototransduction reactions in the rhabdomeric photoreceptor are profoundly stochastic due to the small number of participating molecules and small reaction space. The resulting quantum bumps (QBs) vary in their timing (latency), amplitudes and durations, and these variabilities within each cell are not correlated. Using modeling and electrophysiological recordings, we investigated how the QB properties depend on the cascade speed and how they influence signal transfer. Parametric analysis in the model supported by experimental data revealed that faster cascades elicit larger and narrower QBs with faster onsets and smaller variabilities than slower cascades. Latency dispersion was stronger affected by modification of upstream than downstream activation parameters. The variability caused by downstream modifications closely matched the experimental variability. Frequency response modeling showed that corner frequency is a reciprocal function of the characteristic duration of the multiphoton response, which, in turn, is a non-linear function of QB duration and latency dispersion. All QB variabilities contributed noise but only latency dispersion slowed and spread multiphoton responses, lowering the corner frequency. Using the discovered QB correlations, we evaluated transduction noise for dissimilar species and two extreme adaptation states, and compared it to photon noise. The noise emitted by the cascade was non-additive and depended non-linearly on the interaction between the QB duration and the three QB variabilities. Increased QB duration strongly suppressed both noise and corner frequency. This trade-off might be acceptable for nocturnal but not diurnal species because corner frequency is the principal determinant of information capacity. To offset the increase in noise accompanying the QB narrowing during light adaptation and the response-expanding effect of latency dispersion, the cascade accelerates. This explains the widespread evolutionary tendency of diurnal fliers to have fast phototransduction, especially after light adaptation, which thus appears to be a common adaptation to contain stochasticity, improve SNR and expand the bandwidth.

Comparative transcriptomic analysis primarily explores the molecular mechanism of compound eye formation in Neocaridina denticulata sinensis

“…It is indicated that each ommatidium contains different types of photoreceptor neurons, cone cells, pigment cells, secreted lenses and retinal cells [36][37][38]. Invertebrates' photoreceptor is rhabdomeric type [38][39][40], and the phototransduction process occurs within its. The phototransduction is mediated by a G-protein alpha-q (Gq)-coupled phospholipase C (PLC) signaling cascade among arthropods [16,41].…”

Non-inactivating voltage-activated K+ conductances can increase photoreceptor signaling bandwidth beyond the bandwidth set by phototransduction

“…In flies, phototransduction cascade adapts to light by decreasing the amplitude, latency and duration of QBs [ 31 ]. Shortening of QB latency is accompanied by a decrease in the spread of latencies, which, together with the narrowing of quantum bumps, underlies the shortening of multiphoton impulse response [ 41 , 42 ]. Since light adaptation is caused by LIC and associated with membrane depolarization, i.e.…”