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

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. Author summary Phototransduction cascades in the rhabdomeric photoreceptors of invertebrates and the ciliary photoreceptors of vertebrates, while similar in their first stages, differ in their outcomes and regulation mechanisms. One salient difference is that in the photoreceptors of many insect species the delay of small responses decreases drastically after light adaptation. Here we performed an in-depth analysis of phototransduction in the insect microvillus and discovered hitherto unknown dependencies between the parameters of the cascade output, the quantum bump, and the cascade speed, supported by experimental data. Faster cascades produced faster, larger and narrower quantum bumps with smaller variabilities than slower cascades. We show that the differences in the cascade speed, either between species occupying dissimilar visual ecological niches, or between adaptation states, have profound consequences for photoreceptor signaling. Firstly, narrow and more synchronous bumps produced by fast cascades better transfer higher frequencies contained in visual signals, increasing the photoreceptor bandwidth. Secondly, a decrease in the level of noise due to the cascade acceleration compensates for the loss of signaling accuracy, which occurs when the signal duration decreases. We propose that acceleration of phototransduction is a powerful mechanism in both evolutionary and situational optimization of photoreceptor signaling.