The topography of rods, cones and intrinsically photosensitive retinal ganglion cells in the retinas of a nocturnal (Micaelamys namaquensis) and a diurnal (Rhabdomys pumilio) rodent

. 2018 ; 13 (8) : e0202106. [epub] 20180809

Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid30092025

We used immunocytochemistry to determine the presence and topographical density distributions of rods, cones, and intrinsically photosensitive retinal ganglion cells (ipRGCs) in the four-striped field mouse (Rhabdomys pumilio) and the Namaqua rock mouse (Micaelamys namaquensis). Both species possessed duplex retinas that were rod dominated. In R. pumilio, the density of both cones and rods were high (cone to rod ratio: 1:1.23) and reflected the species' fundamentally diurnal, but largely crepuscular lifestyle. Similarly, the ratio of cones to rods in M. namaquensis (1:12.4) reflected its nocturnal lifestyle. Similar rod density peaks were observed (R. pumilio: ~84467/mm2; M. namaquensis: ~81088/mm2), but a density gradient yielded higher values in the central (~56618/mm2) rather than in the peripheral retinal region (~32689/mm2) in R. pumilio. Two separate cone types (S-cones and M/L-cones) were identified implying dichromatic color vision in the study species. In M. namaquensis, both cone populations showed a centro-peripheral density gradient and a consistent S- to M/L-cone ratio (~1:7.8). In R. pumilio, S cones showed a centro-peripheral gradient (S- to M/L-cone ratio; central: 1:7.8; peripheral: 1:6.8) which appeared to form a visual streak, and a specialized area of M/L-cones (S- to M/L-cone ratio: 1:15) was observed inferior to the optic nerve. The number of photoreceptors per linear degree of visual angle, estimated from peak photoreceptor densities and eye size, were four cones and 15 rods per degree in M. namaquensis and 11 cones and 12 rods per degree in R. pumilio. Thus, in nocturnal M. namaquensis rods provide much finer image sampling than cones, whereas in diurnal/crepuscular R. pumilio both photoreceptor types provide fine image sampling. IpRGCs were comparably sparse in R. pumilio (total = 1012) and M. namaquensis (total = 862), but were homogeneously distributed in M. namaquensis and densest in the dorso-nasal quadrant in R. pumilio. The adaptive significance of the latter needs further investigation.

Zobrazit více v PubMed

Freedman MS, Lucas RJ, Soni B, von Schantz M, Muñoz M, David-Gray Z, et al. Regulation of mammalian circadian behavior by non-rod, non-cone, ocular photoreceptors. Science. 1999;284: 502–504. PubMed

Schmidt TM, Do MTH, Dacey D, Lucas R, Hattar S, Matynia A. Melanopsin-positive intrinsically photosensitive retinal ganglion cells: from form to function. J Neurosci. 2011;31: 16094–16101. 10.1523/JNEUROSCI.4132-11.2011 PubMed DOI PMC

Peichl L. Diversity of mammalian photoreceptor properties: adaptations to habitat and lifestyle? Anat Rec A. 2005;287: 1001–1012. PubMed

Hattar S, Liao HW, Takao M, Berson DM, Yau KW. Melanopsin-containing retinal ganglion cells: architecture, projections, and intrinsic photosensitivity. Science. 2002;295: 1065–1070. 10.1126/science.1069609 PubMed DOI PMC

Semo MA, Peirson S, Lupi D, Lucas RJ, Jeffery G, Foster RG. Melanopsin retinal ganglion cells and the maintenance of circadian and pupillary responses to light in aged rodless/coneless (rd/rd cl) mice. Eur J Neurosci. 2003;17: 1793–1801. PubMed

Lucas RJ, Freedman MS, Muñoz M, Garcia-Fernández JM, Foster RG. Regulation of the mammalian pineal by non-rod, non-cone, ocular photoreceptors. Science. 1999;284: 505–507. PubMed

Lucas RJ, Douglas RH, Foster RG. Characterization of an ocular photopigment capable of driving pupillary constriction in mice. Nat Neurosci. 2001;4: 621–626. 10.1038/88443 PubMed DOI

Dkhissi-Benyahya O, Gronfier C, De Vanssay W, Flamant Cooper HM. Modeling the role of mid-wavelength cones in circadian responses to light. Neuron. 2007;53: 677–687. 10.1016/j.neuron.2007.02.005 PubMed DOI PMC

Altimus CM, Güler AD, Alam NM, Arman AC, Prusky GT, Sampath AP & Hattar S. Rod photoreceptors drive circadian photoentrainment across a wide range of light intensities. Nat Neurosci. 2010;13: 1107–1112. 10.1038/nn.2617 PubMed DOI PMC

Brown TM, Gias C, Hatori M, Keding SR, Semo M, Coffey PJ, et al. Melanopsin contributions to irradiance coding in the thalamo-cortical visual system. PLoS Biol. 2010;8: 2986. PubMed PMC

Weng S, Estevez ME, Berson DM. Mouse ganglion-cell photoreceptors are driven by the most sensitive rod pathway and by both types of cones. PloS One. 2013;8: ee66480 PubMed PMC

Collin SP. A web-based archive for topographic maps of retinal distribution in vertebrates. Clin Exp Optom. 2008;91: 85–95. 10.1111/j.1444-0938.2007.00228.x PubMed DOI

Govardovskii VI, Röhlich P, Szél Á, Khokhlova TV. Cones in the retina of the mongolian gerbil, Meriones unguiculatus: an immunocytochemical and electophysiological study. Vision Res. 1992;32: 19–27. PubMed

Jacobs GH, Calderone JB, Fenwick JA, Krogh K, Williams GA. Visual adaptations in a diurnal rodent, Octodon degus. J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2003;189: 347–361. 10.1007/s00359-003-0408-0 PubMed DOI

Peichl L, Chávez AE, Ocampo A, Mena W, Bozinovic F, Palacios AG. The eye and vision in the subterranean rodent cururo (Spalacopus cyanus, Octodontidae). J Comp Neurol. 2005;486:197–208 10.1002/cne.20491 PubMed DOI

Jacobs GH. The distribution and nature of colour vision among the mammals. Biol Rev. 1993;68: 413–471. PubMed

Kryger Z, Galli-Resta L, Jacobs GH, Reese BE. The topography of rod and cone photoreceptors in the retina of the ground squirrel. Vis Neurosci. 1998;15: 685–691. PubMed

Bobu C, Lahmam M, Vuillez P, Ouarour A, Hicks D. Photoreceptor organisation and phenotypic characterization in retinas of two diurnal rodent species: Potential use as experimental animal models for human vision research. Vision Res. 2008;48: 424–432. 10.1016/j.visres.2007.08.011 PubMed DOI

Gaillard F, Bonfield S, Gilmour GS, Kuny S, Mema SC, Martin BT, et al. Retinal anatomy and visual performance in a diurnal cone-rich laboratory rodent, the Nile grass rat (Arvicanthis niloticus). J Comp Neurol. 2008;510: 525–538. 10.1002/cne.21798 PubMed DOI

Feldman JL, Phillips CJ. Comparative retinal pigment epithelium and photoreceptor ultrastructure in nocturnal and fossorial rodents: the eastern woodrat, Neotoma floridana, and the plains pocket gopher, Geomys bursarius. J Mammal. 1984;65: 231–245.

Szél Á, Röhlich P. Two cone types of rat retina detected by anti-visual pigment antibodies. Exp Eye Res. 1992;55: 47–52. PubMed

Calderone JB, Jacobs GH. Regional variations in the relative sensitivity to UV light in the mouse retina. Vis Neurosci. 1995;12: 463–468. PubMed

Peichl L, Moutairou K. Absence of short-wavelength sensitive cones in the retinae of seals (Carnivora) and African giant rats (Rodentia). Eur J Neurosci. 1998;10: 2586–2594. PubMed

D’Anelo GJ, Glasser A, Wendt M, Williams GA, Osborn DA, Gallagher GR, et al. Visual specialization of an herbivore prey species, the white-tailed deer. Can J Zool. 2008;86: 735–743.

Szél A, Röhlich P, Caffé AR, Van Veen T. Distribution of cone photoreceptors in the mammalian retina. Microsc Res Tech. 1996;35: 445–462. 10.1002/(SICI)1097-0029(19961215)35:6<445::AID-JEMT4>3.0.CO;2-H PubMed DOI

Ahnelt PK, Kolb H. The mammalian photoreceptor mosaic-adaptive design. Prog Retin Eye Res. 2000;19: 711–777. PubMed

Skinner JD, Chimimba CT. The Mammals of the Southern African Subregion. 3rd ed Cape Town: Cambridge University Press, 2005.

Schumann DM, Cooper HM, Hofmeyr MD, Bennett NC. Circadian rhythm of locomotor activity in the four-striped field mouse, Rhabdomys pumilio: a diurnal African rodent. Physiol Behav. 2005;85: 231–239. 10.1016/j.physbeh.2005.03.024 PubMed DOI

Hemmi JM, Grünert U. Distribution of photoreceptor types in the retina of a marsupial, the tammar wallaby (Macropus eugenii). Vis Neurosci. 1999;16: 291–302. PubMed

Petry HM, Erichsen JT, Szél Á. Immunocytochemical identification of photoreceptor populations in the tree shrew retina. Brain Res. 1993;616: 344–350. PubMed

Peichl L, Künzle HE, Vogel P. Photoreceptor types and distributions in the retinae of insectivores. Vis Neurosci. 2000;17: 937–48. PubMed

Hicks D, Molday RS. Differential immunogold-dextran labeling of bovine and frog rod and cone cells using monoclonal antibodies against bovine rhodopsin. Exp Eye Res. 1986;42: 55–71. PubMed

Röhlich P, Szél Á. Binding sites of photoreceptor-specific antibodies COS-1, OS-2 and AO. Curr Eye Res. 1993;12: 935–944. PubMed

Pettigrew JD, Dreher B, Hopkins CS, McCall MJ, Brown M: Peak density and distribution of ganglion cells in the retinae of microchiropteran bats: implication for visual acuity. Brain Behav Evol. 1988;32: 39–56. 10.1159/000116531 PubMed DOI

Hall MI, Ross CF. Eye shape and activity pattern in birds. J Zool. 2007;271: 437–444.

Martin GR. Visual fields and their functions in birds. J Ornithol. 2007;148: 547–562.

Ross CF, Kirk EC. Evolution of eye size and shape in primates. J Hum Evol. 2007;52: 294–313. 10.1016/j.jhevol.2006.09.006 PubMed DOI

Howland HC, Merola S, Basarab JR. The allometry and scaling of the size of vertebrate eyes. Vision Res. 2004;44: 2043–2065. 10.1016/j.visres.2004.03.023 PubMed DOI

Land MF, Nilsson DE. Animal Eyes. 2nd ed Oxford: Oxford University Press; 2012.

Saïdi T, Mbarek S, Chaouacha-Chekir RB, Hicks D. Diurnal rodents as animal models of human central vision: characterisation of the retina of the sand rat Psammomys obsesus. Graefes Arch Clin Exp Ophthalmol. 2007;249: 1029–1037. PubMed

Carter‐Dawson LD, La Vail MM. Rods and cones in the mouse retina. I. Structural analysis using light and electron microscopy. J Comp Neurol. 1979;188: 245–262. 10.1002/cne.901880204 PubMed DOI

Jeon CJ, Strettoi E, Masland RH. The major cell populations of the mouse retina. J Neurosci. 1998;18: 8936–8946. PubMed PMC

Van der Merwe I, Bennett NC, Haim A, Oosthuizen MK. Locomotor activity in the Namaqua rock mouse (Micaelamys namaquesis): entrainment by light manipulations. Can J Zool. 2014;92: 1083–1091.

Szél A, Csorba G, Caffe AR, Szél G, Röhlich P, Van Veen T. Different patterns of retinal cone topography in two genera of rodents, Mus and Apodemus. Cell Tissue Res. 1994;276: 143–50. PubMed

Von Schantz M, Argamaso-Hernan SM, Szél Á, Foster RG. Photopigments and photoentrainment in the Syrian golden hamster. Brain Res. 1997;770: 131–138. PubMed

Lukáts Á, Dkhissi-Benyahya O, Szepessy Z, Röhlich P, Vígh B, Bennett NC, et al. Visual pigment coexpression in all cones of two rodents, the Siberian hamster and the pouched mouse. Invest Ophthalmol Vis Sci. 2002;43: 2468–2473. PubMed

Peichl L, Nemec P, Burda H. Unusual cone and rod properties in subterranean African mole-rats (Rodentia, Bathyergidae). Eur J Neurosci. 2004;19: 1545–1558. 10.1111/j.1460-9568.2004.03263.x PubMed DOI

Kott O, Moritz RE, Šumbera R, Burda H, Němec P. Light propagation in burrows of subterranean rodents: tunnel system architecture but not photoreceptor sensitivity limits light sensation range. J Zool. 2014;294: 68–76.

Henning Y, Mladěnková N, Burda H, Szafranski K, Begall S. Retinal S-opsin dominance in Ansell’s mole-rats (Fukomys anselli) is a consequence of naturally low serum thyroxine. Sci Rep. 2018;8: 4337 10.1038/s41598-018-22705-y PubMed DOI PMC

Wässle H. Parallel processing in the mammalian retina. Nature Rev Neurosci. 2004;5: 747–757. PubMed

Ecker JL, Dumitrescu ON, Wong KY, Alam NM, Chen SK, Gates Le et al. Melanopsin-expressing retinal ganglion-cellphotoreceptors: Cellular diversity and role in pattern vision. Neuron. 2010;67: 49–60. 10.1016/j.neuron.2010.05.023 PubMed DOI PMC

Estevez ME, Fogerson PM, Ilardi MC, Borghuis BG, Chan E, Weng S, et al. Form and function of the M4 cell, an intrinsically photosensitive retinal ganglion cell type contributing to geniculocortical vision. J Neurosci. 2012;32: 13608–13620. 10.1523/JNEUROSCI.1422-12.2012 PubMed DOI PMC

Reifler AN, Chervenak AP, Dolikian ME, Benenati BA, Meyers BS, Demertzis ZD et al. The rat retina has five types of ganglion-cell photoreceptors. Exp Eye Res. 2015;130: 17–28. 10.1016/j.exer.2014.11.010 PubMed DOI PMC

Karnas D, Mordel J, Bonnet D, Pévet P, Hicks D, Meissl H. Heterogeneity of intrinsically photosensitive retinal ganglion cells in the mouse revealed by molecular phenotyping. J Comp Neurol. 2013; 521: 912–932. 10.1002/cne.23210 PubMed DOI

Berson DM, Castrucci AM, Provencio I. Morphology and mosaics of melanopsin‐expressing retinal ganglion cell types in mice. J Comp Neurol. 2010;518: 2405–2422. 10.1002/cne.22381 PubMed DOI PMC

Karnas D, Hicks D, Mordel J, Pévet P, Meissl H. Intrinsic photosensitive retinal ganglion cells in the diurnal rodent, Arvicanthis ansorgei. PloS One 2013;8: e73343 10.1371/journal.pone.0073343 PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...