Processing of single-photon responses in the mammalian On and Off retinal pathways at the sensitivity limit of vision

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
to the Off pathway. On the other hand, the responses of On ganglion cells allow
better intensity discrimination compared to the Off ganglion cell responses
near visual threshold.