Behavioural and physiological limits to vision in mammals

Abstract

Human vision is exquisitely sensitive-a dark-adapted observer is capable of reliably detecting the absorption of a few quanta of light. Such sensitivity requires that the sensory receptors of the retina, rod photoreceptors, generate a reliable signal when single photons are absorbed. In addition, the retina must be able to extract this information and relay it to higher visual centres under conditions where very few rods signal single-photon responses while the majority generate only noise. Critical to signal transmission are mechanistic optimizations within rods and their dedicated retinal circuits that enhance the discriminability of single-photon responses by mitigating photoreceptor and synaptic noise. We describe behavioural experiments over the past century that have led to the appreciation of high sensitivity near absolute visual threshold. We further consider mechanisms within rod photoreceptors and dedicated rod circuits that act to extract single-photon responses from cellular noise. We highlight how these studies have shaped our understanding of brain function and point out several unresolved questions in the processing of light near the visual threshold.This article is part of the themed issue 'Vision in dim light'.

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

“…For pools of rods relevant for behavior, the limiting source of noise depends on the number of rods, detection versus temporal discrimination tasks, and how rod signals are combined or pooled by readout circuits. Finally, our measurements of rod noise indicate that the thermal activation rate of rhodopsin is about half that of previous estimates [7], suggesting that additional noise sources limit behavioral detection sensitivity.…”

“…Three sources contribute to noise in the rod response: thermal isomerization of rhodopsin, continuous current fluctuations, and variability in the single photon response. Past work exploring the implications of rod noise for visual sensitivity has emphasized the importance of thermal isomerizations while largely neglecting the other sources (reviewed by [7]). One reason for this focus is that thermal noise can be easily expressed as a dark light, while other sources of rod noise (or noise downstream of rods) have a more complex relationship to the signal.…”

“…These considerations have strongly shaped the investigation of rod-mediated vision and the mechanisms that support it. More than a century of work shows that dark-adapted human observers can detect weak flashes of light with a sensitivity approaching the limits set by noise in rod photoreceptors [7]. Past work, however, has focused on the ability to detect photons while neglecting the accuracy with which the time of photon absorption is encoded.…”

Vision in dim light: highlights and challenges

“…Moreover, their accessibility for physiological experiments has permitted perhaps our best analysis of nocturnal vision, from the optics right through to the central neural adaptations within the brain that pool noisy signals. In the second review, Field & Sampath [33] explore the remarkable advances in understanding visual processing by the vertebrate retina, taking us from a description of the classic pioneering work that established the thresholds for visual performance in humans and other vertebrates (and led to a realization that photoreceptors can detect single photons of light), right through to our latest research into the mechanisms of visual transduction and the neural circuits of the retina that pool signals from rod photoreceptors.…”

“…Both of these reviews [12,33] highlight an important point: while recent research is finally unravelling the mysteries of dim light vision, this is still an immature field with many open questions. The remaining papers in the issue nevertheless exploit different animal groups (terrestrial insects, animals from the deep sea and terrestrial vertebrates) to address at least a subset of these.…”