Cellular and molecular mechanisms of photoreceptor tuning for prey capture in larval zebrafish

Abstract

Correspondence to t. yoshimatsu@sussex.ac.uk and t.baden@sussex.ac.uk 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 uses the signal from a single cone at a time. For this, UV-detection efficiency is regionally boosted 42-fold. Next, in vivo 2-photon imaging, transcriptomics and computational modelling 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. Finally, this signal is further 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. Together, our results highlight a rich mechanistic toolkit for the tuning of neurons.

What the Zebrafish’s Eye Tells the Zebrafish’s Brain: Retinal Ganglion Cells for Prey Capture and Colour Vision

“…As predicted from work on photoreceptors (Yoshimatsu et al, 2019;Zimmermann et al, 2018), the density of RGCs was elevated in the SZ (Figs. 1C1).…”

“…For efficient coding (Attneave, 1954;Barlow, 1961;Simoncelli and Olshausen, 2001) zebrafish should therefore invest in different sets of functional RGC types to support different aspects of vision across their retinal surface. In agreement, both photoreceptor (Yoshimatsu et al, 2019) and retinal bipolar cell functions (Zimmermann et al, 2018) are asymmetrically distributed across the eye, and feature pronounced reorganisations in the area temporalis (dubbed Strike Zone, SZ (Zimmermann et al, 2018)), which is used for visual prey capture (Bianco et al, 2011;Mearns et al, 2019;Semmelhack et al, 2014;Yoshimatsu et al, 2019;Zimmermann et al, 2018). In contrast, data on structural and functional retinal anisotropies in zebrafish RGCs remains largely outstanding (but see (Robles et al, 2014)).…”

“…Larval zebrafish use a highly asymmetrical retina to process distinct sets of visual features across different parts of visual space (Robles et al, 2014;Yoshimatsu et al, 2019;Zimmermann et al, 2018). In particular, they feature a pronounced acute zone (area temporalis (Schmitt and Dowling, 1999), dubbed "strike zone", SZ; (Zimmermann et al, 2018)) which is used in conjunction with fixational eye movements for visual guided prey capture (Antinucci et al, 2019;Mearns et al, 2019;Semmelhack et al, 2014;Yoshimatsu et al, 2019). However, the anatomical distribution of RGCs across the eye has never been quantified.…”

“…Conceptually reminiscent, a reduced inhibitory tone in the primate fovea is thought to aid signal-to-noise in low-convergence circuits (Baden et al, 2020;Sinha et al, 2017). In view of their need to process the signal from small numbers of cones for visual prey detection (Yoshimatsu et al, 2019), larval zebrafish RGCs might also be expected to benefit from a low-inhibition arrangement in their SZ.…”

“…In fact, wavelength is strongly associated with specific behaviours in zebrafish. For example, the optomotor response is best driven by long wavelength light (Orger and Baier, 2005), while visual guided prey capture capitalises on short-wavelength vision (Yoshimatsu et al, 2019). However, if and how zebrafish visual behaviours build on signals from spectrally selective RGC circuits remains unknown.…”