Animal eyes have evolved to process behaviorally important visual information, but how retinas deal with statistical asymmetries in visual space remains poorly understood. Using hyperspectral imaging in the field, in vivo 2-photon imaging of retinal neurons, and anatomy, here we show that larval zebrafish use a highly anisotropic retina to asymmetrically survey their natural visual world. First, different neurons dominate different parts of the eye and are linked to a systematic shift in inner retinal function: above the animal, there is little color in nature, and retinal circuits are largely achromatic. Conversely, the lower visual field and horizon are color rich and are predominately surveyed by chromatic and color-opponent circuits that are spectrally matched to the dominant chromatic axes in nature. Second, in the horizontal and lower visual field, bipolar cell terminals encoding achromatic and color-opponent visual features are systematically arranged into distinct layers of the inner retina. Third, above the frontal horizon, a high-gain UV system piggybacks onto retinal circuits, likely to support prey capture.
Summary In the eye, the function of same-type photoreceptors must be regionally adjusted to process a highly asymmetrical natural visual world. Here, we show that UV cones in the larval zebrafish area temporalis are specifically tuned for UV-bright prey capture in their upper frontal visual field, which may use the signal from a single cone at a time. For this, UV-photon detection probability is regionally boosted more than 10-fold. Next, in vivo two-photon imaging, transcriptomics, and computational modeling reveal that these cones use an elevated baseline of synaptic calcium to facilitate the encoding of bright objects, which in turn results from expressional tuning of phototransduction genes. Moreover, the light-driven synaptic calcium signal is regionally slowed by interactions with horizontal cells and later accentuated at the level of glutamate release driving retinal networks. These regional differences tally with variations between peripheral and foveal cones in primates and hint at a common mechanistic origin.
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’.
Hyperspectral imaging is a widely used technology for industrial and scientific purposes, but the high cost and large size of commercial setups have made them impractical for most basic research. Here, we designed and implemented a fully open source and low-cost hyperspectral scanner based on a commercial spectrometer coupled to custom optical, mechanical and electronic components. We demonstrate our scanner’s utility for natural imaging in both terrestrial and underwater environments. Our design provides sub-nm spectral resolution between 350–950 nm, including the UV part of the light spectrum which has been mostly absent from commercial solutions and previous natural imaging studies. By comparing the full light spectra from natural scenes to the spectral sensitivity of animals, we show how our system can be used to identify subtle variations in chromatic details detectable by different species. In addition, we have created an open access database for hyperspectral datasets collected from natural scenes in the UK and India. Together with comprehensive online build- and use-instructions, our setup provides an inexpensive and customisable solution to gather and share hyperspectral imaging data.
The eyes of two glacial-relict populations of opossum shrimp Mysis relicta inhabiting the different photic environments of a deep, darkbrown freshwater lake and a variably lit bay of the Baltic Sea differ in their susceptibility to functional depression from strong light exposures. The lake population is much more vulnerable than the sea population. We hypothesized that the difference reflects physiological adaptation mechanisms operating on long time scales rather than genetically fixed differences between the populations. To test this, we studied how acclimation to ultra-slowly increased illumination (on time scales of several weeks to months) affected the resilience of the eyes to bright-light exposures. Light responses of whole eyes were measured by electroretinography, the visualpigment content of single rhabdoms by microspectrophotometry and the structural integrity of photoreceptor cells by electron microscopy (EM). Slow acclimation mitigated and even abolished the depression of photoresponsiveness caused by strong light exposures, making a dramatic difference especially in the lake animals. Still, acclimation in the sea animals was faster and the EM studies suggested intrinsic differences in the dynamics of microvillar membrane cycling. In conclusion, we report a novel form of physiological adaptation to general light levels, effective on the time scale of seasonal changes. It explains part but not all of the differences in light tolerance between the lake and sea populations.
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