Abstract
Visually guided behaviour at its sensitivity limit relies on single-photon responses originating in a small number of rod photoreceptors. For decades, researchers have debated the neural mechanisms and noise sources that underlie this striking sensitivity. To address this question, we need to understand the constraints arising from the retinal output signals provided by distinct retinal ganglion cell types. It has recently been shown in the primate retina that On and Off parasol ganglion cells, the cell types likely to underlie light detection at the absolute visual threshold, differ fundamentally not only in response polarity, but also in the way they handle single-photon responses originating in rods. The On pathway provides the brain with a thresholded, low-noise readout and the Off pathway with a noisy, linear readout. We outline the mechanistic basis of these different coding strategies and analyse their implications for detecting the weakest light signals. We show that high-fidelity, nonlinear signal processing in the On pathway comes with costs: more single-photon responses are lost and their propagation is delayed compared with the Off pathway. On the other hand, the responses of On ganglion cells allow better intensity discrimination compared with the Off ganglion cell responses near visual threshold.This article is part of the themed issue ‘Vision in dim light’.
Highlights
Vision at its sensitivity limit relies on a small number of photons absorbed among hundreds of rod photoreceptors
Guided behaviour at its sensitivity limit relies on single-photon responses originating in a small number of rod photoreceptors
It has recently been shown in the primate retina that On and Off parasol ganglion cells, the cell types likely to underlie light detection at the absolute visual threshold, differ fundamentally in response polarity, and in the way they handle single-photon responses originating in rods
Summary
Vision at its sensitivity limit relies on a small number of photons absorbed among hundreds of rod photoreceptors. 0.3 photoisomerizations per rod per second, R* per rod per second) was still approximately 30 times higher than the level corresponding to the spontaneous activation rate of rhodopsin in mouse rods [41] and far from representative of the conditions comprising detection of the weakest light increments in the dark In those conditions, close to the absolute visual threshold, another mechanism creates a crucial functional difference between the two pathways, as recently described by AlaLaurila & Rieke [16]. The On pathway shows highly nonlinear response properties, whereas the Off pathway is essentially linear (figure 1a,b) The mechanism underlying this asymmetry resides in the last synapse of the On pathway, located between On cone bipolar cells and On RGCs, and operates as a coincidence detector that passes signals only when two or more SPRs occur simultaneously in the receptive field of an On cone bipolar cell consisting of approximately 1000 rods [16].
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