Abstract
One of the fundamental mysteries of the human visual system is the continuous function of cone photoreceptors in bright daylight. As visual pigment is destroyed, or bleached, by light, cones require its rapid regeneration, which in turn involves rapid recycling of the pigment's chromophore. The canonical visual cycle for rod and cone pigments involves recycling of their chromophore from all-trans retinol to 11-cis retinal in the pigment epithelium, adjacent to photoreceptors. However, shortcomings of this pathway indicate the function of a second, cone-specific, mechanism for chromophore recycling. Indeed, biochemical and physiological studies on lower species have described a cone-specific visual cycle in addition to the long-known pigment epithelium pathway. Two important questions remain, however: what is the role of this pathway in the function of mammalian cones, and is it present in higher mammals, including humans? Here, we show that mouse, primate, and human neural retinas promote pigment regeneration and dark adaptation selectively in cones, but not in rods. This pathway supports rapid dark adaptation of mammalian cones and extends their dynamic range in background light independently of the pigment epithelium. This pigment-regeneration mechanism is essential for our daytime vision and appears to be evolutionarily conserved.
MeSH Terms
Animals
Dark Adaptation/physiology
Electroretinography
Humans
Light/adverse effects
Mice
Retinal Cone Photoreceptor Cells/physiology,radiation effects
Retinal Pigments/metabolism
Vision, Ocular/physiology
Vitamin A/metabolism
Chemicals
Retinal Pigments
Vitamin A
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Wang Jin-Shan
Department of Ophthalmology and Visual Sciences, Washington University School of Medicine, St. Louis, MO 63110, USA.
Kefalov Vladimir J
References (20)
20 references, click to expand
-
Muller cells of chicken retina synthesize 11-cis-retinol.
Biochem J. 1992 Aug 1;285 ( Pt 3):907-13
PMID: 1497628
-
Retinoid cycles in the cone-dominated chicken retina.
J Exp Biol. 2005 Nov;208(Pt 21):4151-7
PMID: 16244173
-
A new method for measuring free drug concentration: retinal tissue as a biosensor.
Invest Ophthalmol Vis Sci. 2006 Jun;47(6):2583-8
PMID: 16723474
-
Diseases caused by defects in the visual cycle: retinoids as potential therapeutic agents.
Annu Rev Pharmacol Toxicol. 2007;47:469-512
PMID: 16968212
-
Human gene therapy for RPE65 isomerase deficiency activates the retinoid cycle of vision but with slow rod kinetics.
Proc Natl Acad Sci U S A. 2008 Sep 30;105(39):15112-7
PMID: 18809924
-
An adaptive ERG technique to measure normal and altered dark adaptation in the mouse.
Doc Ophthalmol. 2007 Nov;115(3):155-63
PMID: 17891429
-
Signaling properties of a short-wave cone visual pigment and its role in phototransduction.
J Neurosci. 2007 Sep 19;27(38):10084-93
PMID: 17881515
-
RPE65 is essential for the function of cone photoreceptors in NRL-deficient mice.
Invest Ophthalmol Vis Sci. 2007 Feb;48(2):534-42
PMID: 17251447
-
Vertebrate photoreceptors.
Prog Retin Eye Res. 2001 Jan;20(1):49-94
PMID: 11070368
-
Nrl-knockout mice deficient in Rpe65 fail to synthesize 11-cis retinal and cone outer segments.
Invest Ophthalmol Vis Sci. 2008 Mar;49(3):1126-35
PMID: 18326740
-
Isomerization and oxidation of vitamin a in cone-dominant retinas: a novel pathway for visual-pigment regeneration in daylight.
Neuron. 2002 Sep 26;36(1):69-80
PMID: 12367507
-
Intra-retinal visual cycle required for rapid and complete cone dark adaptation.
Nat Neurosci. 2009 Mar;12(3):295-302
PMID: 19182795
-
Targeted disruption of Müller cell metabolism induces photoreceptor dysmorphogenesis.
Glia. 2000 Nov;32(2):192-204
PMID: 11008218
-
Retinyl ester hydrolase and the visual cycle in the chicken eye.
Am J Physiol. 1995 Dec;269(6 Pt 2):R1346-50
PMID: 8594936
-
Effect of light exposure on the accumulation and depletion of retinyl ester in the chicken retina.
Exp Eye Res. 2006 Oct;83(4):871-6
PMID: 16780835
-
VISUAL ADAPTATION.
Proc R Soc Lond B Biol Sci. 1965 Mar 16;162:20-46
PMID: 14296430
-
Subfunctionalization of a retinoid-binding protein provides evidence for two parallel visual cycles in the cone-dominant zebrafish retina.
J Neurosci. 2008 Aug 13;28(33):8208-16
PMID: 18701683
-
Physiological features of the S- and M-cone photoreceptors of wild-type mice from single-cell recordings.
J Gen Physiol. 2006 Apr;127(4):359-74
PMID: 16567464
-
Biochemistry of visual pigment regeneration: the Friedenwald lecture.
Invest Ophthalmol Vis Sci. 2000 Feb;41(2):337-48
PMID: 10670460
-
Mouse cone photoresponses obtained with electroretinogram from the isolated retina.
Vision Res. 2008 Jan;48(2):264-72
PMID: 18166210