Wiring the retinal circuits activated by light during early development
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  • 作者:Gabriel E Bertolesi (7)
    Carrie L Hehr (7)
    Sarah McFarlane (7)
  • 关键词:c ; fos ; Melanopsin ; Eye ; Vision ; Circadian rhythm ; Xenopus
  • 刊名:Neural Development
  • 出版年:2014
  • 出版时间:December 2014
  • 年:2014
  • 卷:9
  • 期:1
  • 全文大小:2,615 KB
  • 参考文献:1. Tombran-Tink J, Barnstable CJ: / Visual transduction and non-visual light perception. Totowa, N.J: Humana Press; 2008. CrossRef
    2. McNeill DS, Sheely CJ, Ecker JL, Badea TC, Morhardt D, Guido W, Hattar S: Development of melanopsin-based irradiance detecting circuitry. / Neural Dev 2013, 6:8. CrossRef
    3. Hattar S, Liao HW, Takao M, Berson DM, Yau KW: Melanopsin-containing retinal ganglion cells: architecture, projections, and intrinsic photosensitivity. / Science 2002, 295:1065-070. CrossRef
    4. Lucas RJ, Hattar S, Takao M, Berson DM, Foster RG, Yau KW: Diminished pupillary light reflex at high irradiances in melanopsin-knockout mice. / Science 2003, 299:245-47. CrossRef
    5. Ruby NF, Brennan TJ, Xie X, Cao V, Franken P, Heller HC, O'Hara BF: Role of melanopsin in circadian responses to light. / Science 2002, 298:2211-213. CrossRef
    6. Field GD, Chichilnisky EJ: Information processing in the primate retina: circuitry and coding. / Annu Rev Neurosci 2007, 30:1-0. CrossRef
    7. Lupi D, Oster H, Thompson S, Foster RG: The acute light-induction of sleep is mediated by OPN4-based photoreception. / Nat Neurosci 2008, 11:1068-073. CrossRef
    8. Gooley JJ, Lu J, Fischer D, Saper CB: A broad role for melanopsin in nonvisual photoreception. / J Neurosci 2003, 23:7093-106.
    9. Panda S, Provencio I, Tu DC, Pires SS, Rollag MD, Castrucci AM, Pletcher MT, Sato TK, Wiltshire T, Andahazy M, Kay SA, Van Gelder RN, Hogenesch JB: Melanopsin is required for non-image-forming photic responses in blind mice. / Science 2003, 301:525-27. CrossRef
    10. Sollars PJ, Smeraski CA, Kaufman JD, Ogilvie MD, Provencio I, Pickard GE: Melanopsin and non-melanopsin expressing retinal ganglion cells innervate the hypothalamic suprachiasmatic nucleus. / Vis Neurosci 2003, 20:601-10. CrossRef
    11. Brown TM, Gias C, Hatori M, Keding SR, Semo M, Coffey PJ, Gigg J, Piggins HD, Panda S, Lucas RJ: Melanopsin contributions to irradiance coding in the thalamo-cortical visual system. / PLoS Biol 2010, 8:e1000558. CrossRef
    12. Ecker JL, Dumitrescu ON, Wong KY, Alam NM, Chen SK, LeGates T, Renna JM, Prusky GT, Berson DM, Hattar S: Melanopsin-expressing retinal ganglion-cell photoreceptors: cellular diversity and role in pattern vision. / Neuron 2010, 67:49-0. CrossRef
    13. Belenky MA, Smeraski CA, Provencio I, Sollars PJ, Pickard GE: Melanopsin retinal ganglion cells receive bipolar and amacrine cell synapses. / J Comp Neurol 2003, 460:380-93. CrossRef
    14. Wong KY, Dunn FA, Graham DM, Berson DM: Synaptic influences on rat ganglion-cell photoreceptors. / J Physiol 2007, 582:279-96. CrossRef
    15. Altimus CM, Guler 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, 13:1107-112. CrossRef
    16. Lall GS, Revell VL, Momiji H, Al Enezi J, Altimus CM, Guler AD, Aguilar C, Cameron MA, Allender S, Hankins MW, Lucas RJ: Distinct contributions of rod, cone, and melanopsin photoreceptors to encoding irradiance. / Neuron 2010, 66:417-28. CrossRef
    17. Filadelfi AM, Castrucci AM: Comparative aspects of the pineal/melatonin system of poikilothermic vertebrates. / J Pineal Res 1996, 20:175-86. CrossRef
    18. Green CB, Liang MY, Steenhard BM, Besharse JC: Ontogeny of circadian and light regulation of melatonin release in Xenopus laevis embryos. / Brain Res Dev Brain Res 1999, 117:109-16. CrossRef
    19. Jamieson D, Roberts A: Responses of young Xenopus laevis tadpoles to light dimming: possible roles for the pineal eye. / J Exp Biol 2000, 203:1857-867.
    20. Besharse JC, Iuvone PM: Circadian clock in Xenopus eye controlling retinal serotonin N-acetyltransferase. / Nature 1983, 305:133-35. CrossRef
    21. Chaurasia SS, Rollag MD, Jiang G, Hayes WP, Haque R, Natesan A, Zatz M, Tosini G, Liu C, Korf HW, Iuvone PM, Provencio I: Molecular cloning, localization and circadian expression of chicken melanopsin (Opn4): differential regulation of expression in pineal and retinal cell types. / J Neurochem 2005, 92:158-70. CrossRef
    22. Provencio I, Jiang G, De Grip WJ, Hayes WP, Rollag MD: Melanopsin: an opsin in melanophores, brain, and eye. / Proc Natl Acad Sci U S A 1998, 95:340-45. CrossRef
    23. Green CB: Molecular control of Xenopus retinal circadian rhythms. / J Neuroendocrinol 2003, 15:350-54. CrossRef
    24. Bellingham J, Chaurasia SS, Melyan Z, Liu C, Cameron MA, Tarttelin EE, Iuvone PM, Hankins MW, Tosini G, Lucas RJ: Evolution of melanopsin photoreceptors: discovery and characterization of a new melanopsin in nonmammalian vertebrates. / PLoS Biol 2006, 4:e254. CrossRef
    25. Bellingham J, Whitmore D, Philp AR, Wells DJ, Foster RG: Zebrafish melanopsin: isolation, tissue localisation and phylogenetic position. / Brain Res Mol Brain Res 2002, 107:128-36. CrossRef
    26. Dong C, Zhang J, Qiao J, He G: Positive selection and functional divergence after melanopsin gene duplication. / Biochem Genet 2012, 50:235-48. CrossRef
    27. Hanzlicek BW, Peachey NS, Grimm C, Hagstrom SA, Ball SL: Probing inner retinal circuits in the rod pathway: a comparison of c-fos activation in mutant mice. / Vis Neurosci 2004, 21:873-81. CrossRef
    28. Huerta JJ, Llamosas MM, Cernuda-Cernuda R, Garcia-Fernandez JM: Fos expression in the retina of rd/rd mice during the light/dark cycle. / Neurosci Lett 1997, 232:143-46. CrossRef
    29. Pickard GE, Baver SB, Ogilvie MD, Sollars PJ: Light-induced fos expression in intrinsically photosensitive retinal ganglion cells in melanopsin knockout (opn4) mice. / PLoS One 2009, 4:e4984. CrossRef
    30. Sagar SM, Sharp FR: Light induces a Fos-like nuclear antigen in retinal neurons. / Brain Res Mol Brain Res 1990, 7:17-1. CrossRef
    31. Yu MC, Li WW, Liu K, Yew DT: An immunohistochemical study of the c-fos protooncogene in the developing human retina. / Neuroscience 1994, 60:983-87. CrossRef
    32. Deeg KE, Sears IB, Aizenman CD: Development of multisensory convergence in the Xenopus optic tectum. / J Neurophysiol 2009, 102:3392-404. CrossRef
    33. Holt CE: Does timing of axon outgrowth influence initial retinotectal topography in Xenopus? / J Neurosci 1984, 4:1130-152.
    34. Zhang LI, Tao HW, Holt CE, Harris WA, Poo M: A critical window for cooperation and competition among developing retinotectal synapses. / Nature 1998, 395:37-4. CrossRef
    35. Dong W, Lee RH, Xu H, Yang S, Pratt KG, Cao V, Song YK, Nurmikko A, Aizenman CD: Visual avoidance in Xenopus tadpoles is correlated with the maturation of visual responses in the optic tectum. / J Neurophysiol 2009, 101:803-15. CrossRef
    36. Schlamp CL, Nickells RW: Light and dark cause a shift in the spatial expression of a neuropeptide-processing enzyme in the rat retina. / J Neurosci 1996, 16:2164-171.
    37. Gabriel R, Wilhelm M: Structure and function of photoreceptor and second-order cell mosaics in the retina of Xenopus. / Int Rev Cytol 2001, 210:77-20. CrossRef
    38. Viczian AS, Vignali R, Zuber ME, Barsacchi G, Harris WA: XOtx5b and XOtx2 regulate photoreceptor and bipolar fates in the Xenopus retina. / Development 2003, 130:1281-294. CrossRef
    39. Elshatory Y, Everhart D, Deng M, Xie X, Barlow RB, Gan L: Islet-1 controls the differentiation of retinal bipolar and cholinergic amacrine cells. / J Neurosci 2007, 27:12707-2720. CrossRef
    40. Hirsch N, Harris WA: Xenopus Pax-6 and retinal development. / J Neurobiol 1997, 32:45-1. CrossRef
    41. Dyer MA, Livesey FJ, Cepko CL, Oliver G: Prox1 function controls progenitor cell proliferation and horizontal cell genesis in the mammalian retina. / Nat Genet 2003, 34:53-8. CrossRef
    42. Panda S, Nayak SK, Campo B, Walker JR, Hogenesch JB, Jegla T: Illumination of the melanopsin signaling pathway. / Science 2005, 307:600-04. CrossRef
    43. Drivenes O, Soviknes AM, Ebbesson LO, Fjose A, Seo HC, Helvik JV: Isolation and characterization of two teleost melanopsin genes and their differential expression within the inner retina and brain. / J Comp Neurol 2003, 456:84-3. CrossRef
    44. Tomonari S, Takagi A, Akamatsu S, Noji S, Ohuchi H: A non-canonical photopigment, melanopsin, is expressed in the differentiating ganglion, horizontal, and bipolar cells of the chicken retina. / Dev Dyn 2005, 234:783-90. CrossRef
    45. Verra DM, Contin MA, Hicks D, Guido ME: Early onset and differential temporospatial expression of melanopsin isoforms in the developing chicken retina. / Invest Ophthalmol Vis Sci 2011, 52:5111-120. CrossRef
    46. Davies WI, Zheng L, Hughes S, Tamai TK, Turton M, Halford S, Foster RG, Whitmore D, Hankins MW: Functional diversity of melanopsins and their global expression in the teleost retina. / Cell Mol Life Sci 2011, 68:4115-132. CrossRef
    47. Matos-Cruz V, Blasic J, Nickle B, Robinson PR, Hattar S, Halpern ME: Unexpected diversity and photoperiod dependence of the zebrafish melanopsin system. / PLoS One 2011, 6:e25111. CrossRef
    48. Sandbakken M, Ebbesson L, Stefansson S, Helvik JV: Isolation and characterization of melanopsin photoreceptors of Atlantic salmon (Salmo salar). / J Comp Neurol 2012, 520:3727-744. CrossRef
    49. Sekaran S, Lupi D, Jones SL, Sheely CJ, Hattar S, Yau KW, Lucas RJ, Foster RG, Hankins MW: Melanopsin-dependent photoreception provides earliest light detection in the mammalian retina. / Curr Biol 2005, 15:1099-107. CrossRef
    50. Cheng N, Tsunenari T, Yau KW: Intrinsic light response of retinal horizontal cells of teleosts. / Nature 2009, 460:899-03. CrossRef
    51. Cameron MA, Pozdeyev N, Vugler AA, Cooper H, Iuvone PM, Lucas RJ: Light regulation of retinal dopamine that is independent of melanopsin phototransduction. / Eur J Neurosci 2009, 29:761-67. CrossRef
    52. Zhang DQ, Wong KY, Sollars PJ, Berson DM, Pickard GE, McMahon DG: Intraretinal signaling by ganglion cell photoreceptors to dopaminergic amacrine neurons. / Proc Natl Acad Sci U S A 2008, 105:14181-4186. CrossRef
    53. Witkovsky P, Zhang J, Blam O: Dopaminergic neurons in the retina of Xenopus laevis: amacrine vs. interplexiform subtypes and relation to bipolar cells. / Cell Tissue Res 1994, 278:45-6.
    54. Atkinson-Leadbeater K, Bertolesi GE, Hehr CL, Webber CA, Cechmanek PB, McFarlane S: Dynamic expression of axon guidance cues required for optic tract development is controlled by fibroblast growth factor signaling. / J Neurosci 2010, 30:685-93. CrossRef
    55. Witkovsky P: Photoreceptor classes and transmission at the photoreceptor synapse in the retina of the clawed frog, Xenopus laevis. / Microsc Res Tech 2000, 50:338-46. CrossRef
    56. Koyanagi M, Kubokawa K, Tsukamoto H, Shichida Y, Terakita A: Cephalochordate melanopsin: evolutionary linkage between invertebrate visual cells and vertebrate photosensitive retinal ganglion cells. / Curr Biol 2005, 15:1065-069. CrossRef
    57. Dacey DM, Liao HW, Peterson BB, Robinson FR, Smith VC, Pokorny J, Yau KW, Gamlin PD: Melanopsin-expressing ganglion cells in primate retina signal colour and irradiance and project to the LGN. / Nature 2005, 433:749-54. CrossRef
    58. Pegau WS, Gray D, Zaneveld JR: Absorption and attenuation of visible and near-infrared light in water: dependence on temperature and salinity. / Appl Opt 1997, 36:6035-046. CrossRef
    59. Lamb TD: Evolution of phototransduction, vertebrate photoreceptors and retina. / Prog Retin Eye Res 2013, 36:52-19. CrossRef
    60. Mateju K, Sumova A, Bendova Z: Expression and light sensitivity of clock genes Per1 and Per2 and immediate-early gene c-fos within the retina of early postnatal Wistar rats. / J Comp Neurol 2010, 518:3630-644. CrossRef
    61. Jenkins A, Munoz M, Tarttelin EE, Bellingham J, Foster RG, Hankins MW: VA opsin, melanopsin, and an inherent light response within retinal interneurons. / Curr Biol 2003, 13:1269-278. CrossRef
    62. Joo HR, Peterson BB, Dacey DM, Hattar S, Chen SK: Recurrent axon collaterals of intrinsically photosensitive retinal ganglion cells. / Vis Neurosci 2013, 30:175-82. CrossRef
    63. Zhang DQ, Belenky MA, Sollars PJ, Pickard GE, McMahon DG: Melanopsin mediates retrograde visual signaling in the retina. / PLoS One 2012, 7:e42647. CrossRef
    64. Dowling JE, Ehinger B: Synaptic organization of the amine-containing interplexiform cells of the goldfish and Cebus monkey retinas. / Science 1975, 188:270-73. CrossRef
    65. Osborne NN, Patel S, Vigny A: Dopaminergic neurones in various retinas and the postnatal development of tyrosine-hydroxylase immunoreactivity in the rabbit retina. / Histochemistry 1984, 80:389-93. CrossRef
    66. Wagner HJ, Behrens UD: Microanatomy of the dopaminergic system in the rainbow trout retina. / Vision Res 1993, 33:1345-358. CrossRef
    67. Brecha NC, Oyster CW, Takahashi ES: Identification and characterization of tyrosine hydroxylase immunoreactive amacrine cells. / Invest Ophthalmol Vis Sci 1984, 25:66-0.
    68. Wagner HJ, Wulle I: Contacts of dopaminergic interplexiform cells in the outer retina of the blue acara. / Vis Neurosci 1992, 9:325-33. CrossRef
    69. Sernagor E: Retinal development: second sight comes first. / Curr Biol 2005, 15:R556-R559. CrossRef
    70. Sernagor E, Mehta V: The role of early neural activity in the maturation of turtle retinal function. / J Anat 2001, 199:375-83. CrossRef
    71. Lupi D, Sekaran S, Jones SL, Hankins MW, Foster RG: Light-evoked FOS induction within the suprachiasmatic nuclei (SCN) of melanopsin knockout (Opn4?? mice: a developmental study. / Chronobiol Int 2006, 23:167-79. CrossRef
    72. Chang WS, Harris WA: Sequential genesis and determination of cone and rod photoreceptors in Xenopus. / J Neurobiol 1998, 35:227-44. CrossRef
    73. Saha MS, Grainger RM: Early opsin expression in Xenopus embryos precedes photoreceptor differentiation. / Brain Res Mol Brain Res 1993, 17:307-18. CrossRef
    74. Sakaguchi DS, Murphey RK, Hunt RK, Tompkins R: The development of retinal ganglion cells in a tetraploid strain of Xenopus laevis: a morphological study utilizing intracellular dye injection. / J Comp Neurol 1984, 224:231-51. CrossRef
    75. Fahrenkrug J, Nielsen HS, Hannibal J: Expression of melanopsin during development of the rat retina. / Neuroreport 2004, 15:781-84. CrossRef
    76. Tarttelin EE, Bellingham J, Bibb LC, Foster RG, Hankins MW, Gregory-Evans K, Gregory-Evans CY, Wells DJ, Lucas RJ: Expression of opsin genes early in ocular development of humans and mice. / Exp Eye Res 2003, 76:393-96. CrossRef
    77. Nieuwkoop PD, Faber J: / Normal table of Xenopus laevis. Daudin. New York: Garland Science; 1994.
  • 作者单位:Gabriel E Bertolesi (7)
    Carrie L Hehr (7)
    Sarah McFarlane (7)

    7. Department of Cell Biology and Anatomy, Hotchkiss Brain Institute, University of Calgary, 3330 Hospital Dr. NW, Health Sciences Building, Room 2164, Calgary, AB, T2N4N1, Canada
  • ISSN:1749-8104
文摘
Background Light information is sorted by neuronal circuits to generate image-forming (IF) (interpretation and tracking of visual objects and patterns) and non-image-forming (NIF) tasks. Among the NIF tasks, photic entrainment of circadian rhythms, the pupillary light reflex, and sleep are all associated with physiological responses, mediated mainly by a small group of melanopsin-expressing retinal ganglion cells (mRGCs). Using Xenopus laevis as a model system, and analyzing the c-fos expression induced by light as a surrogate marker of neural activity, we aimed to establish the developmental time at which the cells participating in both systems come on-line in the retina. Results We found that the peripheral retina contains 80% of the two melanopsin-expressing cell types we identified in Xenopus: melanopsin-expressing horizontal cells (mHCs; opn4m+/opn4x+/Prox1+) and mRGCs (2.7% of the total RGCs; opn4m+/opn4x+/Pax6+/Isl1), in a ratio of 6:1. Only mRGCs induced c-fos expression in response to light. Dopaminergic (tyrosine hydroxylase-positive; TH+) amacrine cells (ACs) may be part of the melanopsin-mediated circuit, as shown by preferential c-fos induction by blue light. In the central retina, two cell types in the inner nuclear layer (INL) showed light-mediated induction of c-fos expression [(On-bipolar cells (Otx2+/Isl1+), and a sub-population of ACs (Pax6?Isl1?], as well as two RGC sub-populations (Isl1+/Pax6+ and Isl1+/Pax6?. Melanopsin and opsin expression turned on a day before the point at which c-fos expression could first be activated by light (Stage 37/38), in cells of both the classic vision circuit, and those that participate in the retinal component of the NIF circuit. Key to the classic vision circuit is that the component cells engage from the beginning as functional ‘unit circuits-of two to three cells in the INL for every RGC, with subsequent growth of the vision circuit occurring by the wiring in of more units. Conclusions We identified melanopsin-expressing cells and specific cell types in the INL and the RGC layer which induce c-fos expression in response to light, and we determined the developmental time when they become active. We suggest an initial formulation of retinal circuits corresponding to the classic vision pathway and melanopsin-mediated circuits to which they may contribute.

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