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

Abstract

Summary 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.

Colors everywhere: enhanced chromatic processing across the first visual synapse in the zebrafish central brain

“…Also, the responses in the RAs were more color specific than the responses in RGCs, with a tendency for one or two color stimuli to dominate the response.To better probe the variability of the responses, we constructed a linear model to infer the required cone type's gains (amount of response contribution) yielding a given ROI response [15,17] . As has been reported before, gains of the UV cones were considerably higher than those of the other cone types, and blue gains were mostly negative, indicating they have Off polarity [8,(18)(19)(20) ). The distribution of the gains of RGCs and RAs were very similar, so we identified the patterns present in the combinations of gains to probe for potential differences.…”

“…Additionally, their entire eye and nervous system are accessible to imaging, given they are naturally transparent [3][4][5] . Relying on this advantage, recent research has found that, through a set of color specific horizontal, bipolar and retinal ganglion cells (RGCs) [6][7][8] , the eye then relays tetrachromatic information to several retino-recipient areas (RAs) [9,10] . The main RA is the optic tectum, receiving 97% of the RGC axons via the neuropil mass termed Arborization Field 10 (AF10) [11,12] .…”

“…The light sources were selected to broadly sample the range of wavelengths the fish is sensitive to at naturalistic intensities [6] , rather than attempting to isolate and stimulate individual cone types [15] . Projection was from the bottom to stimulate the dorsal retina, which is well suited for color computations as it concentrates many color opponent RGC responses [8] . We utilized two transgenic fish lines, one expressing the fluorescent calcium indicator GCaMP6s [16] in RGC axon terminals, and the other expressing the same indicator in most of the larval central brain (Fig.…”

“…When focusing on AF10 and the optic tectum, we observed that the color computations are more advanced in tectum, as evidenced by improved decoding and better pattern decorrelation over time, while the responses in AF10 followed the stimulus fluctuations more closely. Finally, we compared the color responses to different behaviorally relevant stimuli, and found that color information is available in conjunction with other visual features, speaking in favor of its influence in many zebrafish brain processes.As this is the first report of color processing in the zebrafish central brain [8] , our aim was to characterize its anatomical distribution. RGCs are known to arborize in defined areas of the brain, and there is cumulative evidence pointing to the selectivity of these areas for certain types 10 of responses [32,33] .…”

“…ROIs in these brain areas are also stimulated mostly by a single color, which is not predominant in other brain regions. Further studies will need to address whether the presence of color information in any of these brain regions has a causal role in visual processing.Recently, Zhou et al [8] described the spectral properties of RGC dendrites and somata in the eye of the larval zebrafish. Our results corroborate their finding of mostly Off blue weights and high UV weights in RGCs, and also of simple and complex color opponencies, although the proportions of types we observed are different.…”