Fovea-like Photoreceptor Specializations Underlie Single UV Cone Driven Prey-Capture Behavior in Zebrafish

Takeshi Yoshimatsu,Cornelius Schröder,Noora E Nevala,Philipp Berens,Tom Baden

doi:10.1016/j.neuron.2020.04.021

Takeshi Yoshimatsu, Cornelius Schröder + Show 3 more

Open Access

https://doi.org/10.1016/j.neuron.2020.04.021

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Journal: Neuron	Publication Date: May 29, 2020
Citations: 107	License type: cc-by

Affiliation: University of Sussex, University of Tübingen

Abstract

SummaryIn 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.

Highlights

In vision, photoreceptors drive the retinal network through continuous modulations in synaptic release (Baden et al, 2013a; Heidelberger et al, 2005; Lagnado and Schmitz, 2015; Moser et al, 2020; Regus-Leidig and Brandsta€tter, 2012; Thoreson, 2007)
Withincondition pairwise comparisons across for SZ versus the other three zones are indicated with asterisks (*p < 0.05, ** p < 0.01, and *** p < 0.001, respectively; p value adjustment, Tukey method for comparing a family of four estimates). (F) Light and dark responses from (C) and (D) plotted against each other for equivalent stimulus durations, with 95% confidence intervals indicated. (G and H) Mean calcium responses to increasing-amplitude 5-ms light flashes from darkness, as indicated (G), and quantification with Hill functions fitted (H). (I) Quantification of calcium responses as in (G) and (H) following horizontal cell (HC) blockage using CNQX
In an example recording from the nasal retina, we presented a 12.8-Hz tetrachromatic binary noise stimulus (Zimmermann et al, 2018; STAR Methods) and recorded the glutamate signals from the HC dendrites that innervate a row of neighboring cones (Figure 8D; Video S6)

Summary

Introduction

Photoreceptors drive the retinal network through continuous modulations in synaptic release (Baden et al, 2013a; Heidelberger et al, 2005; Lagnado and Schmitz, 2015; Moser et al, 2020; Regus-Leidig and Brandsta€tter, 2012; Thoreson, 2007). In the vertebrate retina, the slow rod photoreceptors typically have large outer segments and high-gain intracellular signaling cascades to deliver single-photon sensitivity critical for vision at low light (Field et al, 2005; Lamb, 2016; Yau and Hardie, 2009). Matching the properties of a given photoreceptor type to a specific set of sensory tasks critically underpins vision. These visual requirements can differ dramatically across the retinal surface and the corresponding position in visual space (Baden et al, 2013b; Hardie, 1984; Land and Nilsson, 2012; Sancer et al, 2019; Yilmaz and Meister, 2013; Zimmermann et al, 2018). For efficient sampling (Cronin et al, 2014; Land and Nilsson, 2012), even cones of a single type must be functionally tuned depending on their retinal location

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