Zebrafish Retinal Ganglion Cells Asymmetrically Encode Spectral and Temporal Information across Visual Space

• Published in: Current biology Vol. 30; no. 15; pp. 2927 - 2942.e7
• Main Authors: Zhou, Mingyi, Bear, John, Roberts, Paul A., Janiak, Filip K., Semmelhack, Julie, Yoshimatsu, Takeshi, Baden, Tom
• Format: Journal Article
• Language: English
• Published: England Elsevier Inc 03.08.2020; Cell Press
• Subjects: 2P imaging; Animals; Behavior, Animal; Brain - physiology; color vision; Color Vision - physiology; larval zebrafish; Photic Stimulation; prey capture; retina; Retina - cytology; Retina - embryology; retinal ganglion cells; Retinal Ganglion Cells - physiology; Spatial Processing - physiology; Ultraviolet Rays; UV-vision; Zebrafish - physiology; 2P imaging; retina; larval zebrafish; retinal ganglion cells; prey capture; UV-vision; color vision
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2020.05.055

In vertebrate vision, the tetrachromatic larval zebrafish permits non-invasive monitoring and manipulating of neural activity across the nervous system in vivo during ongoing behavior. However, despite a perhaps unparalleled understanding of links between zebrafish brain circuits and visual behaviors, comparatively little is known about what their eyes send to the brain 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 corresponding with asymmetries in the statistics of natural visual space and behavioral demands. Here, we use in vivo two-photon imaging during hyperspectral visual stimulation as well as photolabeling of RGCs to provide a 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 color opponency, including many that are driven by a pervasive and slow blue-Off system—far in excess of what would be required to satisfy traditional models of color vision. In addition, most information on spectral contrast was intermixed with temporal information. Taken together, our results suggest that zebrafish RGCs send a diverse and highly regionalized time-color code to the brain. [Display omitted] •The structure and function of larval zebrafish RGCs are highly position dependent•The acute zone is dominated by broadly stratifying slow UV-On cells•Approximately half of all RGCs display diverse forms of spectral opponency•Much spectral opponency is driven by a pervasive slow blue-Off system Zhou, Bear et al. chart the functional diversity of retinal ganglion cells in larval zebrafish by imaging responses to spectrally naturalistic full-field stimuli in the in vivo eye. This reveals substantial regionalization, including a UV dominance in the acute zone, and the presence of a pervasive, spectrally opponent slow blue-Off system.