Ganglion cells in larval zebrafish retina integrate inputs from multiple cone types.

We recently showed the presence of seven physiological cone opsins-R1 (575 nm), R2 (556 nm), G1 (460 nm), G3 (480 nm), B1 (415 nm), B2 (440 nm), and UV (358 nm)-in electroretinogram (ERG) recordings of larval zebrafish (Danio rerio) retina. Larval ganglion cells (GCs) are generally thought to integrate only four cone opsin signals (red, green, blue, and UV). We address the question as to whether they may integrate seven cone spectral signals. Here we examined the 127 possible combinations of seven cone signals to find the optimal representation, as based on impulse discharge data sets from GC axons in the larval optic nerve. We recorded four varieties of light-response waveform, sustained-ON, transient-ON, ON-OFF, and OFF, based on the time course of mean discharge rates to all stimulus wavelengths combined. Modeling of GC responses revealed that each received 1-6 cone opsin signals, with a mean of 3.8 ± 1.3 cone signals/GC. Most onset or offset responses were opponent (ON, 80%; OFF, 100%). The most common cone signals were UV (93%), R2 (50%), G3 (55%), and G1 (60%). Seventy-three percent of cone opsin signals were excitatory, and 27% were inhibitory. UV signals favored excitation, whereas G3 and B2 signals favored inhibition. R1/R2, G1/G3, and B1/B2 opsin signals were selectively associated along a nonsynergistic/opponent axis. Overall, these results suggest that larval zebrafish GC spectral responses are complex and use inputs from the seven expressed opsins.NEW & NOTEWORTHY Ganglion cells in larval zebrafish retina have complex spectral responses driven by seven different cone opsin types. UV cone inputs are significant and excitatory to ganglion cells, whereas green and blue cone inputs favor inhibition. Most dramatic are the pentachromatic cells. These responses were identified at 5-6 days after fertilization, reflecting an impressive level of color processing not seen in older fish or mammals.