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.

Inhibition Controls Receptive Field Size, Sensitivity, and Response Polarity of Direction Selective Ganglion Cells Near the Threshold of Vision

“…The absolute sensitivity of each DSGC was quantified as the fraction of correctly discriminated trials in which a flash was presented ('flash' trials) from trials during which no stimulus was presented ('no flash' trials). The discrimination was performed using a 2AFC analysis (Chichilnisky and Rieke, 2005;Dhingra and Smith, 2004;Field et al, 2019). The response in each trial was summarized by a vector, which specified the spike count as a function of time (in 20 ms bins).…”

“…A model of rod responses and was used to test how differences in RF size across DSGCs impacts their predicted thresholds to just detectable flashes in a 2AFC task. The simulation and pooling of rod signals was examined by using a recently published model of rod responses (Field et al, 2019). The model includes specific factors to capture the three dominant noise sources in the rod photocurrent: continuous fluctuations in the dark current (a.k.a.…”

“…Continuous dark noise, ( ), was generated by sampling from a Gaussian distribution and filtering in time to match the power spectrum of measured continuous noise (Field et al, 2019). N photon responses in an individual rod were generated by the first term in Eq.…”

“…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 E ( ), and the covariance of the single photon response is captured by summing over a weighted set, wi, of eigenvectors, G ( ), derived from the covariance matrix of the single photon response (Field et al, 2019). Finally, discrete noise events caused by the thermal activation of rhodopsin were captured by the second term of Eq.…”

“…In the original formulation of this model (Field et al, 2019), the noise parameters were derived from measurements of the photocurrent from primate rods. We adjusted these parameters to account for the greater amounts of continuous noise and variability in the single-photon response present in mouse rods (both relative to the amplitude of the mean single-photon response).…”