Abstract
Neural circuits associated with retinal ganglion cells have long been used as models for investigating the mechanisms that govern circuit development and function. Similar to neurons in the brain, retinal ganglion cells are subdivided into distinct classes based upon their morphology, physiology, and patterns of connectivity. Newly developed transgenic tools in which individual classes of retinal ganglion cells are labeled with reporter proteins have recently provided a method to study the development of their class-specific circuitry. Here, we examine a single class of intrinsically photosensitive retinal ganglion cells and discuss their class-specific circuitry, as well as the cellular and molecular mechanisms that govern assembly of this circuitry.
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Masland RH (2001) The fundamental plan of the retina. Nat Neurosci 4:877–886
Sanes JR, Zipursky SL (2010) Design principles of insect and vertebrate visual systems. Neuron 66:15–36
Masland RH (2001) Neuronal diversity in the retina. Curr Opin Neurobiol 11:431–436
Volgyi B, Chheda S, Bloomfield SA (2009) Tracer coupling patterns of the ganglion cell subtypes in the mouse retina. J Comp Neurol 512:664–687
Muscat L, Huberman AD, Jordan CL, Morin LP (2003) Crossed and uncrossed retinal projections to the hamster circadian system. J Comp Neurol 466:513–524
Hattar S, Kumar M, Park A, Tong P, Tung J, Yau KW, Berson DM (2006) Central projections of melanopsin-expressing retinal ganglion cells in the mouse. J Comp Neurol 497:326–349
Drager UC, Olsen JF (1980) Origins of crossed and uncrossed retinal projections in pigmented and albino mice. J Comp Neurol 191:383–412
Kay JN, De la Huerta I, Kim IJ, Zhang Y, Yamagata M, Chu MW, Meister M, Sanes JR (2011) Retinal ganglion cells with distinct directional preferences differ in molecular identity, structure, and central projections. J Neurosci 31:7753–7762
Kim IJ, Zhang Y, Yamagata M, Meister M, Sanes JR (2008) Molecular identification of a retinal cell type that responds to upward motion. Nature 452:478–482
Kim IJ, Zhang Y, Meister M, Sanes JR (2010) Laminar restriction of retinal ganglion cell dendrites and axons: subtype-specific developmental patterns revealed with transgenic markers. J Neurosci 30:1452–1462
Huberman AD, Manu M, Koch SM, Susman MW, Lutz AB, Ullian EM, Baccus SA, Barres BA (2008) Architecture and activity-mediated refinement of axonal projections from a mosaic of genetically identified retinal ganglion cells. Neuron 59:425–438
Huberman AD, Wei W, Elstrott J, Stafford BK, Feller MB, Barres BA (2009) Genetic identification of an On–Off direction-selective retinal ganglion cell subtype reveals a layer-specific subcortical map of posterior motion. Neuron 62:327–334
Rivlin-Etzion M, Zhou K, Wei W, Elstrott J, Nguyen PL, Barres BA, Huberman AD, Feller MB (2011) Transgenic mice reveal unexpected diversity of on–off direction-selective retinal ganglion cell subtypes and brain structures involved in motion processing. J Neurosci 31:8760–8769
Yonehara K, Shintani T, Suzuki R, Sakuta H, Takeuchi Y, Nakamura-Yonehara K, Noda M (2008) Expression of SPIG1 reveals development of a retinal ganglion cell subtype projecting to the medial terminal nucleus in the mouse. PLoS One 3:e1533
Yonehara K, Ishikane H, Sakuta H, Shintani T, Nakamura-Yonehara K, Kamiji NL, Usui S, Noda M (2009) Identification of retinal ganglion cells and their projections involved in central transmission of information about upward and downward image motion. PLoS One 4:e4320
Badea TC, Cahill H, Ecker J, Hattar S, Nathans J (2009) Distinct roles of transcription factors brn3a and brn3b in controlling the development, morphology, and function of retinal ganglion cells. Neuron 61:852–864
Hattar S, Liao HW, Takao M, Berson DM, Yau KW (2002) Melanopsin-containing retinal ganglion cells: architecture, projections, and intrinsic photosensitivity. Science 295:1065–1070
Ecker JL, Dumitrescu ON, Wong KY, Alam NM, Chen SK, LeGates T, Renna JM, Prusky GT, Berson DM, Hattar S (2010) Melanopsin-expressing retinal ganglion-cell photoreceptors: cellular diversity and role in pattern vision. Neuron 67:49–60
Foster RG, Provencio I, Hudson D, Fiske S, De Grip W, Menaker M (1991) Circadian photoreception in the retinally degenerate mouse (rd/rd). J Comp Physiol A 169:39–50
Provencio I, Wong S, Lederman AB, Argamaso SM, Foster RG (1994) Visual and circadian responses to light in aged retinally degenerate mice. Vision Res 34:1799–1806
Czeisler CA, Shanahan TL, Klerman EB, Martens H, Brotman DJ, Emens JS, Klein T, Rizzo JF 3rd (1995) Suppression of melatonin secretion in some blind patients by exposure to bright light. N Engl J Med 332:6–11
Freedman MS, Lucas RJ, Soni B, von Schantz M, Munoz M, David-Gray Z, Foster R (1999) Regulation of mammalian circadian behavior by non-rod, non-cone, ocular photoreceptors. Science 284:502–504
Provencio I, Jiang G, De Grip WJ, Hayes WP, Rollag MD (1998) Melanopsin: an opsin in melanophores, brain, and eye. Proc Natl Acad Sci USA 95:340–345
Provencio I, Rodriguez IR, Jiang G, Hayes WP, Moreira EF, Rollag MD (2000) A novel human opsin in the inner retina. J Neurosci 20:600–605
Lucas RJ, Douglas RH, Foster RG (2001) Characterization of an ocular photopigment capable of driving pupillary constriction in mice. Nat Neurosci 4:621–626
Gooley JJ, Lu J, Chou TC, Scammell TE, Saper CB (2001) Melanopsin in cells of origin of the retinohypothalamic tract. Nat Neurosci 4:1165
Berson DM, Dunn FA, Takao M (2002) Phototransduction by retinal ganglion cells that set the circadian clock. Science 295:1070–1073
Gooley JJ, Lu J, Fischer D, Saper CB (2003) A broad role for melanopsin in nonvisual photoreception. J Neurosci 23:7093–7106
Provencio I, Rollag MD, Castrucci AM (2002) Photoreceptive net in the mammalian retina. This mesh of cells may explain how some blind mice can still tell day from night. Nature 415:493
Panda S, Sato TK, Castrucci AM, Rollag MD, DeGrip WJ, Hogenesch JB, Provencio I, Kay SA (2002) Melanopsin (Opn4) requirement for normal light-induced circadian phase shifting. Science 298:2213–2216
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 (2003) Melanopsin is required for non-image-forming photic responses in blind mice. Science 301:525–527
Zhang DQ, Wong KY, Sollars PJ, Berson DM, Pickard GE, McMahon DG (2008) Intraretinal signaling by ganglion cell photoreceptors to dopaminergic amacrine neurons. Proc Natl Acad Sci USA 105:14181–14186
Baver SB, Pickard GE, Sollars PJ, Pickard GE (2008) Two types of melanopsin retinal ganglion cell differentially innervate the hypothalamic suprachiasmatic nucleus and the olivary pretectal nucleus. Eur J Neurosci 27:1763–1770
Berson DM, Castrucci AM, Provencio I (2010) Morphology and mosaics of melanopsin-expressing retinal ganglion cell types in mice. J Comp Neurol 518:2405–2422
Schmidt TM, Kofuji P (2009) Functional and morphological differences among intrinsically photosensitive retinal ganglion cells. J Neurosci 29:476–482
Viney TJ, Balint K, Hillier D, Siegert S, Boldogkoi Z, Enquist LW, Meister M, Cepko CL, Roska B (2007) Local retinal circuits of melanopsin-containing ganglion cells identified by transsynaptic viral tracing. Curr Biol 17:981–988
Dacey DM, Liao HW, Peterson BB, Robinson FR, Smith VC, Pokorny J, Yau KW, Gamlin PD (2005) Melanopsin-expressing ganglion cells in primate retina signal colour and irradiance and project to the LGN. Nature 433:749–754
Schmidt TM, Kofuji P (2011) Structure and function of bistratified intrinsically photosensitive retinal ganglion cells in the mouse. J Comp Neurol 519:1492–1504
Perez-Leon JA, Warren EJ, Allen CN, Robinson DW, Lane BR (2006) Synaptic inputs to retinal ganglion cells that set the circadian clock. Eur J Neurosci 24:1117–1123
Wong KY, Dunn FA, Graham DM, Berson DM (2007) Synaptic influences on rat ganglion-cell photoreceptors. J Physiol 582:279–296
Belenky MA, Smeraski CA, Provencio I, Sollars PJ, Pickard GE (2003) Melanopsin retinal ganglion cells receive bipolar and amacrine cell synapses. J Comp Neurol 460:380–393
Hoshi H, Liu WL, Massey SC, Mills SL (2009) ON inputs to the OFF layer: bipolar cells that break the stratification rules of the retina. J Neurosci 29:8875–8883
Dumitrescu ON, Pucci FG, Wong KY, Berson DM (2009) Ectopic retinal ON bipolar cell synapses in the OFF inner plexiform layer: contacts with dopaminergic amacrine cells and melanopsin ganglion cells. J Comp Neurol 517:226–244
Grunert U, Jusuf PR, Lee SC, Nguyen DT (2010) Bipolar input to melanopsin containing ganglion cells in primate retina. Vis Neurosci 28:39–50
Ostergaard J, Hannibal J, Fahrenkrug J (2007) Synaptic contact between melanopsin-containing retinal ganglion cells and rod bipolar cells. Invest Ophthalmol Vis Sci 48:3812–3820
Muller LP, Do MT, Yau KW, He S, Baldridge WH (2010) Tracer coupling of intrinsically photosensitive retinal ganglion cells to amacrine cells in the mouse retina. J Comp Neurol 518:4813–4824
Contini M, Lin B, Kobayashi K, Okano H, Masland RH, Raviola E (2010) Synaptic input of ON-bipolar cells onto the dopaminergic neurons of the mouse retina. J Comp Neurol 518:2035–2050
Sanes JR, Yamagata M (2009) Many paths to synaptic specificity. Annu Rev Cell Dev Biol 25:161–195
Zipursky SL, Sanes JR (2011) Chemoaffinity revisited: dscams, protocadherins, and neural circuit assembly. Cell 143:343–353
Tran TS, Kolodkin AL, Bharadwaj R (2007) Semaphorin regulation of cellular morphology. Annu Rev Cell Dev Biol 23:263–292
Matsuoka RL, Nguyen-Ba-Charvet KT, Parray A, Badea TC, Chedotal A, Kolodkin AL (2011) Transmembrane semaphorin signalling controls laminar stratification in the mammalian retina. Nature 470:259–263
Suto F, Tsuboi M, Kamiya H, Mizuno H, Kiyama Y, Komai S, Shimizu M, Sanbo M, Yagi T, Hiromi Y, Chedotal A, Mitchell KJ, Manabe T, Fujisawa H (2007) Interactions between plexin-A2, plexin-A4, and semaphorin 6A control lamina-restricted projection of hippocampal mossy fibers. Neuron 53:535–547
Runker AE, Little GE, Suto F, Fujisawa H, Mitchell KJ (2008) Semaphorin-6A controls guidance of corticospinal tract axons at multiple choice points. Neural Dev 3:34
Su J, Haner CV, Imbery TE, Brooks JM, Morhardt DR, Gorse K, Guido W, Fox MA (2011) Reelin is required for class-specific retinogeniculate targeting. J Neurosci 31:575–586
McNeill DS, Sheely CJ, Ecker JL, Badea TC, Morhardt D, Guido W, Hattar S (2011) Development of melanopsin-based irradiance detecting circuitry. Neural Dev 6:8
Morin LP, Blanchard JH, Provencio I (2003) Retinal ganglion cell projections to the hamster suprachiasmatic nucleus, intergeniculate leaflet, and visual midbrain: bifurcation and melanopsin immunoreactivity. J Comp Neurol 465:401–416
Sperry RW (1944) Optic nerve regeneration with return of vision in anurans. J Neurophysiol 7:57–69
Sperry RW (1963) Chemoaffinity in the orderly growth of nerve fiber patterns and connections. Proc Natl Acad Sci USA 50:703–710
Huberman AD, Feller MB, Chapman B (2008) Mechanisms underlying development of visual maps and receptive fields. Annu Rev Neurosci 31:479–509
D'Arcangelo G, Miao GG, Chen SC, Soares HD, Morgan JI, Curran T (1995) A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature 374:719–723
Del Rio JA, Heimrich B, Borrell V, Forster E, Drakew A, Alcantara S, Nakajima K, Miyata T, Ogawa M, Mikoshiba K, Derer P, Frotscher M, Soriano E (1997) A role for Cajal–Retzius cells and reelin in the development of hippocampal connections. Nature 385:70–74
Borrell V, Del Rio JA, Alcantara S, Derer M, Martinez A, D'Arcangelo G, Nakajima K, Mikoshiba K, Derer P, Curran T, Soriano E (1999) Reelin regulates the development and synaptogenesis of the layer-specific entorhino-hippocampal connections. J Neurosci 19:1345–1358
Borrell V, Pujadas L, Simo S, Dura D, Sole M, Cooper JA, Del Rio JA, Soriano E (2007) Reelin and mDab1 regulate the development of hippocampal connections. Mol Cell Neurosci 36:158–173
Sheldon M, Rice DS, D'Arcangelo G, Yoneshima H, Nakajima K, Mikoshiba K, Howell BW, Cooper JA, Goldowitz D, Curran T (1997) Scrambler and yotari disrupt the disabled gene and produce a reeler-like phenotype in mice. Nature 389:730–733
Howell BW, Hawkes R, Soriano P, Cooper JA (1997) Neuronal position in the developing brain is regulated by mouse disabled-1. Nature 389:733–737
Renna JM, Weng S, Berson DM (2011) Light acts through melanopsin to alter retinal waves and segregation of retinogeniculate afferents. Nat Neurosci 14:827–829
Chen SK, Badea TC, Hattar S (2011) Photoentrainment and pupillary light reflex are mediated by distinct populations of ipRGCs. Nature 17. doi:10.1038/nature10206
Do MT, Yau KW (2010) Intrinsically photosensitive retinal ganglion cells. Physiol Rev 90:1547–1581
Acknowledgments
Work in our laboratories is supported by grants from the National Institutes of Health [NIH; EY012716 (WG) and EY021222 (MAF)], the Thomas F. Jeffress and Kate Miller Jeffress Memorial Trust (MAF), the A.D. Williams Fund (MAF), and the VCU Presidential Research Incentive Fund (MAF).
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Fox, M.A., Guido, W. Shedding Light on Class-Specific Wiring: Development of Intrinsically Photosensitive Retinal Ganglion Cell Circuitry. Mol Neurobiol 44, 321–329 (2011). https://doi.org/10.1007/s12035-011-8199-8
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DOI: https://doi.org/10.1007/s12035-011-8199-8