Preprint Review Version 1 Preserved in Portico This version is not peer-reviewed

­The Retinal Basis of Vertebrate Color Vision

Version 1 : Received: 19 November 2018 / Approved: 20 November 2018 / Online: 20 November 2018 (11:14:49 CET)

How to cite: Baden, T.; Osorio, D. ­The Retinal Basis of Vertebrate Color Vision. Preprints 2018, 2018110498. https://doi.org/10.20944/preprints201811.0498.v1 Baden, T.; Osorio, D. ­The Retinal Basis of Vertebrate Color Vision. Preprints 2018, 2018110498. https://doi.org/10.20944/preprints201811.0498.v1

Abstract

Vertebrate color vision is evolutionarily ancient. Jawless fish evolved four main spectral types of cone photoreceptor, almost certainly complemented by retinal circuits to process chromatic opponent signals. Subsequent evolution of photoreceptors and visual pigments are now documented for many vertebrate lineages and species, giving insight into evolutionary variation and ecological adaptation of color vision. We look at organization of the photoreceptor mosaic and the functions different types of cone in teleost fish, primates, and birds and reptiles. By comparison less is known about the underlying neural processing. Here we outline the diversity of vertebrate color vision and summarize our understanding of how spectral information picked up by animal photoreceptor arrays is adapted to natural signals. We then turn to the question of how spectral information is processed in the retina. Here, the quite well known and comparatively ‘simple’ system of mammals such as mice and primates reveals some evolutionarily conserved features such as the mammalian BlueON system which compares short and long wavelength receptors signals. We then survey our current understanding of the more complex circuits of fish, amphibians, birds and reptiles. Together, these clades make up more than 90% of vertebrate species, yet we know disturbingly little about their neural circuits for colour vision beyond the photoreceptors. Here, long-standing work on goldfish, freshwater turtles and other species is being complemented by new insights gained from the experimentally amendable retina of zebrafish. From this body of work, one thing is clear: The retinal basis of colour vision in non-mammalian vertebrates is substantially richer compared to mammals: Diverse and complex spectral tunings are established at the level of the cone output via horizontal cell feedforward circuits. From here, zebrafish use cone-selective wiring in bipolar cells to set-up color opponent synaptic layers in the inner retina, which in turn lead a large diversity of color-opponent channels for transmission to the brain. However, while we are starting to build an understanding of the richness of spectral properties in some of these species’ retinal neurons, little is known about inner retinal connectivity and cell-type identify. To gain an understanding of their actual circuits, and thus to build a more generalised understanding of the vertebrate retinal basis of color vision, it will be paramount to expand ongoing efforts in deciphering the retinal circuits of non-mammalian models.

Keywords

color vision; cone photoreceptors; opponency; retina

Subject

Biology and Life Sciences, Animal Science, Veterinary Science and Zoology

Comments (0)

Comment 1
Received: 26 November 2018
Commenter: David Lagman
The commenter has declared there is no conflict of interests.
Comment: Hi,

I have just read your preprint review and found it very interesting since i have been working in the field of vertebrate colour vision evolution during my PhD studies. I have a comment about the evolution of rhodopsin as well as the other vertebrate visual opsins. Our previous research suggest that RH1, RH2, SWS1 and SWS2 all originate from an ancestral gene that duplicated in the two early vertebrate genome duplications, based on analyses on chromosomal regions in several species. The presence of all of these genes in some lamprey species would thus suggest that those duplications took place before the split of jawed and jawless vertebrates and not after as you suggest in the preprint. Below i have provided a list of papers from that work that might be of interest to you if you haven't read it previously.

All the best,
David

Evolution and expression of the phosphodiesterase 6 genes unveils vertebrate novelty to control photosensitivity.
Lagman D, Franzén IE, Eggert J, Larhammar D, Abalo XM.
BMC Evol Biol. 2016 Jun 13;16(1):124. doi: 10.1186/s12862-016-0695-z.
PMID: 27296292

Transducin duplicates in the zebrafish retina and pineal complex: differential specialisation after the teleost tetraploidisation.
Lagman D, Callado-Pérez A, Franzén IE, Larhammar D, Abalo XM.
PLoS One. 2015 Mar 25;10(3):e0121330. doi: 10.1371/journal.pone.0121330. eCollection 2015.
PMID: 25806532

The vertebrate ancestral repertoire of visual opsins, transducin alpha subunits and oxytocin/vasopressin receptors was established by duplication of their shared genomic region in the two rounds of early vertebrate genome duplications.
Lagman D, Ocampo Daza D, Widmark J, Abalo XM, Sundström G, Larhammar D.
BMC Evol Biol. 2013 Nov 2;13:238. doi: 10.1186/1471-2148-13-238.
PMID: 24180662

Expansion of transducin subunit gene families in early vertebrate tetraploidizations.
Lagman D, Sundström G, Ocampo Daza D, Abalo XM, Larhammar D.
Genomics. 2012 Oct;100(4):203-11. doi: 10.1016/j.ygeno.2012.07.005. Epub 2012 Jul 17.
PMID: 22814267

Evolution of vertebrate rod and cone phototransduction genes.
Larhammar D, Nordström K, Larsson TA.
Philos Trans R Soc Lond B Biol Sci. 2009 Oct 12;364(1531):2867-80. doi: 10.1098/rstb.2009.0077. Review.
PMID: 19720650

Extensive duplications of phototransduction genes in early vertebrate evolution correlate with block (chromosome) duplications.
Nordström K, Larsson TA, Larhammar D.
Genomics. 2004 May;83(5):852-72.
PMID: 15081115
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