SUMMARY In the vertebrate visual system, all output of the retina is carried by retinal ganglion cells. Each type encodes distinct visual features in parallel for transmission to the brain. How many such “output channels” exist and what each encodes is an area of intense debate. In mouse, anatomical estimates range between 15–20 channels, and only a handful are functionally understood. Combining two-photon calcium imaging to obtain dense retinal recordings and unsupervised clustering of the resulting sample of >11,000 cells, we here show that the mouse retina harbours substantially more than 30 functional output channels. These include all known and several new ganglion cell types, as verified by genetic and anatomical criteria. Therefore, information channels from the mouse’s eye to the mouse’s brain are considerably more diverse than shown thus far by anatomical studies, suggesting an encoding strategy resembling that used in state-of-the-art artificial vision systems.

SUMMARY The retina extracts visual features for transmission to the brain. Different types of bipolar cell split the photoreceptor input into parallel channels and provide the excitatory drive for downstream visual circuits. Anatomically and genetically, mouse bipolar cell types have been described at great detail, but a similarly deep understanding of their functional diversity is lacking. By imaging light-driven glutamate release from more than 13,000 bipolar cell axon terminals in the intact retina, we here show that bipolar cell functional diversity is generated by the interplay of dendritic excitatory inputs and axonal inhibitory inputs. The resultant centre and surround components of bipolar cell receptive fields interact to decorrelate bipolar cell output in the spatial and temporal domain. Our findings highlight the importance of inhibitory circuits in generating functionally diverse excitatory pathways and suggest that decorrelation of parallel visual pathways begins already at the second synapse of the mouse visual system.

Color vision is essential for an animal's survival. It starts in the retina, where signals from different photoreceptor types are locally compared by neural circuits. Mice, like most mammals, are dichromatic with two cone types. They can discriminate colors only in their upper visual field. In the corresponding ventral retina, however, most cones display the same spectral preference, thereby presumably impairing spectral comparisons. In this study, we systematically investigated the retinal circuits underlying mouse color vision by recording light responses from cones, bipolar and ganglion cells. Surprisingly, most color-opponent cells are located in the ventral retina, with rod photoreceptors likely being involved. Here, the complexity of chromatic processing increases from cones towards the retinal output, where non-linear center-surround interactions create specific color-opponent output channels to the brain. This suggests that neural circuits in the mouse retina are tuned to extract color from the upper visual field, aiding robust detection of predators and ensuring the animal's survival.