Amacrine cells differentially balance zebrafish colour circuits in the central and peripheral retina

In vertebrate vision, the feature-extracting circuits of the inner retina
are driven by photoreceptors whose outputs are already pre-processed. In
zebrafish, for example, outer retinal circuits split “colour” from
“greyscale” information across all four cone-photoreceptor types. How does
the inner retina process this incoming spectral information while also
combining cone signals to shape new greyscale functions? We address this
question by imaging the light-driven responses of amacrine cells (ACs) and
bipolar cells (BCs) in larval zebrafish, in the presence and
pharmacological absence of inner retinal inhibition. We find that amacrine
cells exert distinct effects on greyscale processing depending on retinal
region, as well as contributing to the generation of colour opponency in
the central retina. However, in the peripheral retina amacrine cells
enhanced opponency in some bipolar cells while at the same time
suppressing pre-existing opponency in others, such that the net change in
the number of colour-opponent units was essentially zero. To achieve this
‘dynamic balance’ ACs counteracted intrinsic colour opponency of BCs via
the On-channel. Consistent with these observations, Off-stratifying ACs
were exclusively achromatic, while all colour opponent ACs stratified in
the On-sublamina. This study reveals that the central and peripheral
retina of larval zebrafish employ fundamentally distinct inhibitory
circuits to control the interaction between greyscale- and
colour-processing. Differential actions on the On- and Off-channels
control the transmission of colour-opponent signals in the periphery.