Temporal resolution of single-photon responses in primate rod photoreceptors and limits imposed by cellular noise

Abstract

Sensory receptor noise corrupts sensory signals, contributing to imperfect perception and dictating central processing strategies. For example, noise in rod phototransduction limits our ability to detect light, and minimizing the impact of this noise requires precisely tuned nonlinear processing by the retina. But detection sensitivity is only one aspect of night vision: prompt and accurate behavior also requires that rods reliably encode the timing of photon arrivals. We show here that the temporal resolution of responses of primate rods is much finer than the duration of the light response and identify the key limiting sources of transduction noise. We also find that the thermal activation rate of rhodopsin is lower than previous estimates, implying that other noise sources are more important than previously appreciated. A model of rod single-photon responses reveals that the limiting noise relevant for behavior depends critically on how rod signals are pooled by downstream neurons. NEW & NOTEWORTHY Many studies have focused on the visual system’s ability to detect photons, but not on its ability to encode the relative timing of detected photons. Timing is essential for computations such as determining the velocity of moving objects. Here we examine the timing precision of primate rod photoreceptor responses and show that it is more precise than previously appreciated. This motivates an evaluation of whether scotopic vision approaches limits imposed by rod temporal resolution.

The cGMP Pathway and Inherited Photoreceptor Degeneration: Targets, Compounds, and Biomarkers

“…In the phototransduction cascade, in the dark, high levels of cGMP in photoreceptor outer segments (OS) allow for the sensitization of photoreceptor cells down to the level of single-photon sensitivity [12]. cGMP binds to and opens the prototypic phototransduction target, the cyclic nucleotide-gated channel (CNGC), located in the outer membrane of the photoreceptor OS [13].…”

The mammalian rod synaptic ribbon is essential for Cavchannel facilitation and ultrafast fusion of the readily releasable pool of vesicles

“…Better insight into these matters will further our understanding of how rods convert depolarizations into synaptic signals, and ultimately how the mammalian rod pathway encodes object motion and position (Tikidji-Hamburyan et al, 2017;Field et al, 2019).…”

Properties of multi-vesicular release from rod photoreceptors support transmission of single photon responses

“…To model the rod photocurrent and the detection sensitivity limits set by photocurrent noise sources (Fig. 8), we used a generative model of the rod response (Field et al, 2019). A rod response, r(t) , was generated from the following equation: Continuous dark noise, η ( t ), was generated by sampling from a Gaussian distribution and filtered in time to match the power spectrum of measured continuous noise (Field et al, 2019).…”

“…2 by sampling from a Poisson distribution with a mean given by the flash strength on a given trial. The mean single photon response is given by r μ ( t ), and the covariance of the single photon response is captured by summing over a weighted set, w i , of eigenvectors, c i ( t ), derived from the covariance matrix of the single photon response (Field et al, 2019).…”

“…The kinetics of the single photon response and the shape of the power spectrum of the continuous noise are both similar between mouse and primate rods, so no adjustments were made to these quantities. The thermal rate in mammalian and mouse rods is somewhat uncertain, with the literature allowing for a wide range of values between 0.001 and 0.015 Rh*/rod/s, so we chose an intermediate value of 0.005 Rh*/rod/s (Burns et al, 2002; Field et al, 2019; Fu et al, 2008; Yue et al, 2017). Importantly, this model for simulating rod responses reproduces rod detection and temporal sensitivities in a two-alternative forced-choice (2AFC) task (Field et al, 2019), supporting the application of this model for analyzing task performance of pools of rods.…”