UV-cones differentially encode contrast in vivo to support distinct visual functions across visual space

Abstract

Purpose : Different parts of the retina survey different regions of visual space. For efficient sampling, retinal circuits must therefore adjust their function depending on the position within the retina. Here we show that in larval zebrafish, this specialisation is already exquisitely fine-tuned in the cones. UV-cones that occupy different regions in the retina vary in size, and in addition use different synaptic calcium levels and ribbon designs to specifically tune their contrast-response functions to best support prey capture, UV-based colour vision and predator detection.

Methods : We used in vivo 2-photon imaging of Ca²⁺ and glutamate responses from individual UV-cones across different positions in the eye. We expressed (i) SyGCaMP6f in UV cones for Ca²⁺ imaging, (ii) iGluSnFR in postsynaptic horizontal cells (HCs) and mCherry in UV for glutamate, and (iii) jRGeco1b in UV together with iGluSnFR in HCs for simultaneous recording of both Ca²⁺ and glutamate. Next, to computationally explore the precise sites for functional tuning of UV synaptic transfer functions, we used Bayesian inference to simultaneously fit 7 parameters to a computational model that link Ca²⁺ to synaptic release, including vesicle pool sizes, their dynamics and their Ca²⁺ affinities. Finally, to experimentally verify model predictions, we explored ribbon geometries across different position of UV cones using an Airyscan super-resolution microscope.

Results : We find that UV-cones in different parts of the eye are both structurally and functionally distinct from each other. UV in the ventro-temporal retina that is used for prey capture of UV-bright microorganisms (“strike zone”, SZ) had the largest outer segments and responded equally to light- and dark- flashes. In contrast, ventral and dorsal UV-cones, which serve predator detection against a bright background were much smaller and responded near exclusively to dark flashes. Nasal UV-cones, which are critical for UV-based colour vision along the chromatically rich visual horizon, as well as predator detection, were intermediate between SZ and dorsal/ventral cones. Many of these high-level properties could be systematically attributed to specific tuning steps at the level of calcium regulation and ribbon structure.

Conclusions : Our results show that how photoreceptors can tune their synaptic machineries to implement specialised functions in the different parts of the retina.

This abstract was presented at the 2019 ARVO Annual Meeting, held in Vancouver, Canada, April 28 - May 2, 2019.