The presence of two spectrally different kinds of rod photoreceptors in amphibians has been hypothesized to enable purely rod-based colour vision at very low light levels. The hypothesis has never been properly tested, so we performed three behavioural experiments at different light intensities with toads (Bufo) and frogs (Rana) to determine the thresholds for colour discrimination. The thresholds of toads were different in mate choice and prey-catching tasks, suggesting that the differential sensitivities of different spectral cone types as well as task-specific factors set limits for the use of colour in these behavioural contexts. In neither task was there any indication of rod-based colour discrimination. By contrast, frogs performing phototactic jumping were able to distinguish blue from green light down to the absolute visual threshold, where vision relies only on rod signals. The remarkable sensitivity of this mechanism comparing signals from the two spectrally different rod types approaches theoretical limits set by photon fluctuations and intrinsic noise. Together, the results indicate that different pathways are involved in processing colour cues depending on the ecological relevance of this information for each task.This article is part of the themed issue ‘Vision in dim light’.
Highlights d Diurnal effects on visual sensitivity were studied from the retina to behavior d Visually guided behavior of mice reaches the highest sensitivity at night d The sensitivity limit of retinal ganglion cells does not show diurnal differences d Mice use a better search strategy for visual cues at night
Many animals rely on vision to navigate through their environment. The pattern of changes in the visual scene induced by self-motion is the optic flow, which is first estimated in local patches by directionally selective (DS) neurons. But how should the arrays of DS neurons, each responsive to motion in a preferred direction at a specific retinal position, be organized to support robust decoding of optic flow by downstream circuits? Understanding this global organization is challenging because it requires mapping fine, local features of neurons across the animal's field of view. InDrosophila, the asymmetric dendrites of the T4 and T5 DS neurons establish their preferred direction, making it possible to predict DS responses from anatomy. Here we report that the preferred directions of fly DS neurons vary at different retinal positions and show that this spatial variation is established by the anatomy of the compound eye. To estimate the preferred directions across the visual field, we reconstructed hundreds of T4 neurons in a full brain EM volume and discovered unexpectedly stereotypical dendritic arborizations that are independent of location. We then used whole-head μCT scans to map the viewing directions of all compound eye facets and found a non-uniform sampling of visual space that explains the spatial variation in preferred directions. Our findings show that the organization of preferred directions in the fly is largely determined by the compound eye, exposing an intimate and unexpected connection between the peripheral structure of the eye, functional properties of neurons deep in the brain, and the control of body movements.
SUMMARYPerception of light in darkness requires no more than a handful of photons and this remarkable behavioral performance can be directly linked to a particular retinal circuit – the retinal ON pathway. However, the neural limits to shadow detection in very dim light have remained unresolved. Here, we unravel the neural mechanisms that determine the sensitivity of mice to the dimmest light decrements by measuring signals from the most sensitive ON and OFF retinal ganglion cell types and by correlating their signals with visually guided behavior. We show that mice can detect shadows when only a few photon absorptions are missing among thousands of rods. Behavioral detection of “quantal” shadows relies only on the retinal OFF pathway and is limited by noise and losses of single-photon signals in retinal processing. Thus, in the dim-light regime, light increments and decrements are encoded separately via the ON and OFF retinal pathways, respectively.
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