Birds multiplex spectral and temporal visual information via retinal On- and Off-channels

Abstract

Early retinal circuits divide incoming visual information into functionally opposite elementary signals: On and Off, transient and sustained, chromatic and achromatic. Together these signals can yield an efficient representation of the scene for transmission to the brain via the optic nerve. For example, primate On- and Off-parasol circuits are transient, while On- and Off-midget circuits are sustained. But this long-standing interpretation of retinal function is based on mammals, and it is unclear whether this functional arrangement is common to all vertebrates. Here we show that poultry chicks use a fundamentally different strategy to communicate information from the eye to the brain. Rather than using functionally opposite pairs of retinal output channels, chicks encode the polarity, timing, and spectral composition of visual stimuli in a highly correlated manner: fast achromatic information is encoded by Off-circuits, and slow chromatic information overwhelmingly by On-circuits. Moreover, most retinal output channels combine On- and Off-circuits to simultaneously encode, or multiplex, both achromatic and chromatic information. Our results from birds conform to evidence from fish, amphibians, and reptiles which retain the full ancestral complement of four spectral types of cone photoreceptors. By contrast, mammals lost two of these cones early in their evolution, and we posit that this loss drove a radical simplification and reorganisation of retinal circuits, while birds and many other extant non-mammalian lineages retain the ancestral strategy for retinal image processing. HIGHLIGHTSO_LIFirst large-scale survey of visual functions in an avian retina C_LIO_LIOff-circuits are fast and achromatic, On-circuits are slow and chromatic C_LIO_LIMost avian RGCs are OnOff and encode both types of information C_LIO_LIColour and greyscale information can be decoded based on the kinetics C_LI