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

Abstract

In vertebrate vision, the tetrachromatic larval zebrafish permits non-invasive monitoring and manipulating of neural activity across the nervous system in vivo during ongoing behaviour. However, despite a perhaps unparalleled understanding of links between zebrafish brain circuits and visual behaviours, comparatively little is known about what their eyes send to the brain in the first place via retinal ganglion cells (RGCs). Major gaps in knowledge include any information on spectral coding, and information on potentially critical variations in RGC properties across the retinal surface to acknowledge asymmetries in the statistics of natural visual space and behavioural demands. Here, we use in vivo two photon (2P) imaging during hyperspectral visual stimulation as well as photolabeling of RGCs to provide the first eye-wide functional and anatomical census of RGCs in larval zebrafish. We find that RGCs’ functional and structural properties differ across the eye and include a notable population of UV-responsive On-sustained RGCs that are only found in the acute zone, likely to support visual prey capture of UV-bright zooplankton. Next, approximately half of RGCs display diverse forms of colour opponency - long in excess of what would be required to satisfy traditional models of colour vision. However, most information on spectral contrast was intermixed with temporal information. To consolidate this series of unexpected findings, we propose that zebrafish may use a novel “dual-achromatic” strategy segregated by a spectrally intermediate background subtraction system. Specifically, our data is consistent with a model where traditional achromatic image-forming vision is mainly driven by long-wavelength sensitive circuits, while in parallel UV-sensitive circuits serve a second achromatic system of foreground-vision that serves prey capture and, potentially, predator evasion.