In vertebrate vision, the feature extracting circuits of the inner retina are driven by heavily pre-processed photoreceptor signals. For example, in larval zebrafish, outer retinal circuits serve to split "colour" from "greyscale" information across their four ancestral cone–photoreceptor types. How then can the inner retina simultaneously preserve such incoming spectral information despite the need to combine cone-signals to shape new greyscale functions? To address this question, we imaged light-driven signals from the axon terminals of retinal bipolar cells in the presence and pharmacological absence of inhibition from amacrine cells. Surprisingly, this manipulation had no net effect on the inner retinal representation of colour-opponency, despite profound impacts on all tested greyscale functions such as the gain and kinetics of bipolar cell light responses. This "dynamic balance" was achieved by amacrine cells driving opponency in some bipolar cells, while at the same time suppressing pre-existing opponency in others, such that the net change across the network was essentially zero. To do so, amacrine cells near-exclusively leveraged the On-channel, and correspondingly, a direct in vivo survey of amacrine cell functions revealed that all their colour-opponent responses were located in the On-layer. In contrast, Off-stratifying amacrine cells were largely achromatic. We conclude that complex interactions within the inner retina that underlie greyscale visual processing tasks are intricately balanced via the On-channel to not notably alter the pre-existing population representation of colour information.