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

Abstract

In vertebrate vision, 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. However, 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 male 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.

From water to land: Evolution of photoreceptor circuits for vision in air

“…Double cones are usually also the largest and most numerous cone types, which maximises their potential for temporal and spatial resolution, respectively [ 63 ]. In support, birds generally have some of the fastest eyes of any vertebrate [ 64 ], and the spectral tuning of birds’ fastest retinal output channels ( Fig 3C ) is consistent with a primary drive from a red opsin expressing cone [ 65 ]. However, the extent to which these fast channels are driven by red single and/or double cones remains unknown.…”

“…Based on our still very limited understanding of retinal coding outside of mammals, the "visual way" of eutherians appears to be diametrically opposite to that of most fish and their diverse non-eutherian descendants including birds [65]. Eutherians tend to represent On and Off or fast and slow signals via parallel streams, with only a minority of neurons occupying the coding space in between these extremes [65,[84][85][86][87].…”

“…( c ) Mean spike rates of 2 functionally identified ganglion cell clusters from poultry chick retina in response to a time-accelerating full field chirp stimulus as indicated (mod. from ref [ 65 ]). ( d ) As (a), but for frogs, who lost ancestral green cones (RH2) but evolved “blue rods.” Potentially, blue rods serve functions similar to those served by ancestral blue cones of fish, however at lower light levels.…”

A heterogeneous population code at the first synapse of vision

“…Notably, the disproportionate representation of large negative contrasts (as opposed to positive contrasts) may be an “accident of design” driven by the fact that vertebrate photoreceptors are Off cells (the same basic strategy would also work for On-photoreceptors disproportionately representing large positive contrasts), and may link with the observation that Off-circuits tend to disproportionately represent several elementary aspects of visual scene, including fast temporal contrasts and spectrally broad achromatic signals 40,41,72,73 . Accordingly, while various types of dark-biases in vertebrate retinal encoding have been linked to statistical dark-biases in some 35,74 but not all 6,9,10,75 natural scenes, it seems reasonable to include the intrinsic polarity bias of vertebrate photoreceptors as a key contributor.…”

“…The striking emphasis on the transient signalling of negative contrasts rather than positive at the output of red cones (Fig. 4E) may contribute to the observation that downstream retinal Off-circuits tend to transmit higher frequencies than On [39][40][41] . To investigate the temporal filters at red cone synapses we measured responses to a "chirp" stimulus in which the frequency of a fullfield sinusoid (100% contrast) was swept from 20 Hz to 1 Hz over a period of 20 s. To assess the variability in the timing of responses, we next presented a 20 Hz sinusoidal stimulus at 100% contrast for 30 s (Fig.…”