What the avian eye tells its brain: processing of chromatic and achromatic information at the level of chicken retinal ganglion cells

Birds have highly sophisticated vision, including tetrachromacy but it is unknown how visual information is processed within the retina. Using a high density multielectrode, stimulus driven extracellular electrical signals of multiple retinal ganglion cells (RGC) were measured in parallel. Twenty-seven functionally distinct RGC types were identified by clustering, revealing major principles of avian RGC electrophysiology: Firstly, most RGCs were excited by both ON and OFF steps, and had complex chromatic sensitivities and opponency responses, often in combination with wavelength dependent and long response latencies in the ON channel. These RGCs resemble small bistratified (blue-ON) RGCs in the primate retina. A second group of RGCs showed OFF dominant responses, faster response latencies, and simpler spectral sensitivities, likely matching double cones. These cells potentially form a classical achromatic contrast pathway, like primate alpha/parasol RGCs. Focusing on wavelength dependent response latencies, we found that except for near UV responses, long wavelength ON-responses yielded the shortest latency and most synchronised responses, consistently followed by shorter wavelengths. Combining these insights, we used principal component analysis of flash-responses to reveal that greyscale and “colour” stimuli are encoded in a near-orthogonal manner. We tentatively suggest that birds use a combination of time- and opponency-coding to represent spectral information, while a smaller proportion of cells act as fast greyscale OFF channels which serve achromatic vision.