Spectral inference reveals principal cone-integration rules of the zebrafish inner retina

Abstract

Highlights d Three axes of spectral opponency are encoded by larval zebrafish bipolar cells d The two longer wavelength opponent axes are probably inherited from cones d The short-wavelength opponent axis is probably built in the inner retina d This third opponent axis may link with S-cone opponent circuit in mammals

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

“…Mammals 49,66 and elasmobranchs 67 are also unusual among vertebrates in that most of their bipolar cells and RGCs are mono-or at most bistratified, rather than routinely multistratified as is the case in birds 20,32 , reptiles 68 , amphibians 69 , and fish 10,70,71 . In view of the well-documented links between inner retinal depth, response polarity, and kinetics 3,5,6,12,36,72 , these anatomical differences may directly feed into the observed functional differences. Future functional exploration of other vertebrate retinas, especially those that like mammals have lost a subset of their original photoreceptor complement, may be instructive.…”

“…Alternatively, narrow tuning could be built by rectifying an already opponent input. For example, a hypothetical RGC rectifying an incoming drive from a colour opponent BC 12,36,79 such that only the On-lobe of the opponency persists could readily account for the profusion of 'colour-selective' On-RGCs in our dataset. Neurons with similar properties have long been discussed as part of the colour vision machinery of the primate cortex, where they are usually referred to as hue-selective 80 .…”

“…These long-standing principles are overwhelmingly based on research on mammals, such as mice, primates, cats, and rabbits, and evidence from non-mammalian species is beginning to question their generality. For example, zebrafish lack the approximately balanced representations of On-and Off-, and of transient and sustained channels of mammalian retinas [10][11][12][13][14][15][16] . Similarly, the profusion of colouropponent responses in turtles 17 , or the heavy dominance of OnOff channels in salamanders 18,19 , do not easily map onto the current framework.…”

The vertebrate retina: a window into the evolution of computation in the brain

“…However, this also means that from studying mammals alone, it is not possible to tell if alpha circuits are categorically red cone driven, or if ancestrally they might have integrated more broadly across available photoreceptors. Here, a quick look at zebrafish and chicken, who both retain the full four-cone ancestral photoreceptor complement 54 , 67 , hints that the red cone–dominated drive is in fact the ancestral state for alphas; fast Off circuits in these species are almost exclusively red cone driven 30 , 51 , 52 , 60 , 73 , despite the easy availability of several other cone types. This tentatively suggests that there is a benefit of keeping these very ‘general’ alpha channels free from excessive cone pooling.…”