Form and function of the M4 cell, an intrinsically photosensitive retinal ganglion cell type contributing to geniculocortical vision

Journal of Neuroscience

Volumn 32, Issue 39, 2012, Pages 13608-13620

  Estevez, Maureen E ^a   Michelle Fogerson, P ^a   Ilardi, Marissa C ^a   Borghuis, Bart G ^b   Chan, Eric ^a,c   Weng, Shijun ^a,d   Auferkorte, Olivia N ^a,e   Demb, Jonathan B ^b   Berson, David M ^a  

^a BROWN UNIVERSITY   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c ROCKEFELLER UNIVERSITY   (United States)

^d FUDAN UNIVERSITY   (China)

^e MAX PLANCK INSTITUTE FOR BRAIN RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MELANOPSIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL STRUCTURE; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; ELECTRORETINOGRAPHY; EVOKED VISUAL RESPONSE; FEMALE; GENICULATE NUCLEUS; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; M4 CELL; MALE; MOUSE; NONHUMAN; PATCH CLAMP; PHOTOSENSITIVITY; PHOTOSTIMULATION; PRIORITY JOURNAL; RETINA GANGLION CELL; RETINA RECEPTIVE FIELD; SPIKE WAVE; SYNAPTIC TRANSMISSION;

ACTINS; ANIMALS; BETA-GALACTOSIDASE; CHOLERA TOXIN; CHOLINE O-ACETYLTRANSFERASE; DENDRITES; ELECTRORETINOGRAPHY; FEMALE; GENICULATE BODIES; GREEN FLUORESCENT PROTEINS; LIGHT; MALE; MEMBRANE POTENTIALS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PATCH-CLAMP TECHNIQUES; PHOTIC STIMULATION; RETINA; RETINAL GANGLION CELLS; ROD OPSINS; VISUAL CORTEX; VISUAL FIELDS; VISUAL PATHWAYS;

EID: 84866661603     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1422-12.2012     Document Type: Article

References (57)

1. Allen AE, Brown TM, Lucas RJ (2011) A distinct contribution of shortwavelength-sensitive cones to light-evoked activity in the mouse pretectal olivary nucleus. J Neurosci 31:16833-16843.
2. Applebury ML, Antoch MP, Baxter LC, Chun LL, Falk JD, Farhangfar F, Kage K, Krzystolik MG, Lyass LA, Robbins JT (2000) The murine cone photoreceptor: a single cone type expresses both S and M opsins with retinal spatial patterning. Neuron 27:513-523.
3. Badea TC, Nathans J (2004) Quantitative analysis of neuronal morphologies in the mouse retina visualized by using a genetically directed reporter. J Comp Neurol 480:331-351.
4. 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.
5. Berson DM (2008) Retinal ganglion cell types and their central projections. In: The senses: a comprehensive reference (Masland RH, Albright TD, eds), pp 491-520. San Diego: Academic.
6. Berson DM, Dunn FA, Takao M (2002) Phototransduction by retinal ganglion cells that set the circadian clock. Science 295:1070-1073.
7. 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.
8. Boycott BB, Wässle H (1974) The morphological types of ganglion cells of the domestic cat's retina. J Physiol 240:397-419.
9. Brown TM, Gias C, Hatori M, Keding SR, Semo M, Coffey PJ, Gigg J, Piggins HD, Panda S, Lucas RJ (2010) Melanopsin contributions to irradiance coding in the thalamo-cortical visual system. PLoS Biol 8:e1000558.
10. Brown TM, Tsujimura S, Allen AE, Wynne J, Bedford R, Vickery G, Vugler A, Lucas RJ (2012) Melanopsin-based brightness discrimination in mice and humans. Curr Biol 22:1134-1141.
11. Cleland BG, Levick WR, Wässle H (1975) Physiological identification of a morphological class of cat retinal ganglion cells. J Physiol 248:151-171.
12. Coombs J, van der List D, Wang GY, Chalupa LM (2006) Morphological properties of mouse retinal ganglion cells. Neuroscience 140:123-136.
13. Crook JD, Peterson BB, Packer OS, Robinson FR, Troy JB, Dacey DM (2008a) Y-cell receptive field and collicular projection of parasol ganglion cells in macaque monkey retina. J Neurosci 28:11277-11291.
14. Crook JD, Peterson BB, Packer OS, Robinson FR, Gamlin PD, Troy JB, Dacey DM (2008b) The smooth monostratified ganglion cell: evidence for spatial diversity in the Y-cell pathway to the lateral geniculate nucleus and superior colliculus in the macaque monkey. J Neurosci 28:12654-12671.
15. 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.
16. Demb JB, Zaghloul K, Haarsma L, Sterling P (2001) Bipolar cells contribute to nonlinear spatial summation in the brisk-transient (Y) ganglion cell in mammalian retina. J Neurosci 21:7447-7454.
17. Do MT, Kang SH, Xue T, Zhong H, Liao HW, Bergles DE, Yau KW (2009) Photon capture and signalling by melanopsin retinal ganglion cells. Nature 457:281-287.
18. 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.
19. Ekesten B, Gouras P, Yamamoto S (2000) Cone inputs to murine retinal ganglion cells. Vision Res 40:2573-2577.
20. Enroth-Cugell C, Robson JG (1966) The contrast sensitivity of retinal ganglion cells of the cat. J Physiol 187:517-552.
21. Famiglietti EV (2004) Class I and class II ganglion cells of rabbit retina: a structural basis for X and Y (brisk) cells. J Comp Neurol 478:323-346.
22. Fischer QS, Graves A, Evans S, Lickey ME, Pham TA (2007) Monocular deprivation in adult mice alters visual acuity and single-unit activity. Learn Mem 14:277-286.
23. Hatori M, Le H, Vollmers C, Keding SR, Tanaka N, Buch T, Waisman A, Schmedt C, Jegla T, Panda S (2008) Inducible ablation of melanopsinexpressing retinal ganglion cells reveals their central role in non-image forming visual responses. PLoS ONE 3:e2451.
24. Hattar S, Liao HW, Takao M, Berson DM, Yau KW (2002) Melanopsincontaining retinal ganglion cells: architecture, projections, and intrinsic photosensitivity. Science 295:1065-1070.
25. 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.
26. Heikkinen H, Nymark S, Koskelainen A (2008) Mouse cone photoresponses obtained with electroretinogram from the isolated retina. Vision Res 48:264-272.
27. Hochstein S, Shapley RM (1976) Linear and nonlinear spatial subunits in Y cat retinal ganglion cells. J Physiol 262:265-284.
28. 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.
29. Koehler CL, Akimov NP, Rentería RC (2011) Receptive field center size decreases and firing properties mature in ON and OFF retinal ganglion cells after eye opening in the mouse. J Neurophysiol 106:895-904.
30. Kolesnikov AV, Tang PH, Parker RO, Crouch RK, Kefalov VJ (2011) The mammalian cone visual cycle promotes rapid M/L-cone pigment regeneration independently of the interphotoreceptor retinoid-binding protein. J Neurosci 31:7900-7909.
31. Luan L, Ren C, Lau BW, Yang J, Pickard GE, So KF, Pu M (2011) Y-like retinal ganglion cells innervate the dorsal Raphe nucleus in the Mongolian gerbil (Meriones unguiculatus). PLoS One 6:e18938.
32. Manookin MB, Beaudoin DL, Ernst ZR, Flagel LJ, Demb JB (2008) Disinhibition combines with excitation to extend the operating range of the OFF visual pathway in daylight. J Neurosci 28:4136-4150.
33. Murphy GJ, Rieke F (2006) Network variability limits stimulus-evoked spike timing precision in retinal ganglion cells. Neuron 52:511-524.
34. Nikonov SS, Kholodenko R, Lem J, Pugh EN Jr (2006) Physiological features of the S- and M-cone photoreceptors of wild-type mice from singlecell recordings. J Gen Physiol 127:359-374.
35. Nymark S, Heikkinen H, Haldin C, Donner K, Koskelainen A (2005) Light responses and light adaptation in rat retinal rods at different temperatures. J Physiol 567:923-938.
36. Panda S, Nayak SK, Campo B, Walker JR, Hogenesch JB, Jegla T (2005) Illumination of the melanopsin signaling pathway. Science 307:600-604.
37. Pang JJ, Gao F, Wu SM (2003) Light-evoked excitatory and inhibitory synaptic inputs to ON and OFF alpha ganglion cells in the mouse retina. J Neurosci 23:6063-6073.
38. Paxinos G, Franklin KBJ (2001) The mouse brain in stereotaxic coordinates. San Diego: Academic.
39. Peichl L (1991) Alpha ganglion cells in mammalian retinae: common properties, species differences, and some comments on other ganglion cells. Vis Neurosci 7:155-169.
40. Pfeiffenberger C, Yamada J, Feldheim DA (2006) Ephrin-As and patterned retinal activity act together in the development of topographic maps in the primary visual system. J Neurosci 26:12873-12884.
41. Pu M, Berson DM, Pan T (1994) Structure and function of retinal ganglion cells innervating the cat's geniculate wing: an in vitro study. J Neurosci 14:4338-4358.
42. Qiu X, Kumbalasiri T, Carlson SM, Wong KY, Krishna V, Provencio I, Berson DM (2005) Induction of photosensitivity by heterologous expression of melanopsin. Nature 433:745-749.
43. Remtulla S, Hallett PE (1985) A schematic eye for the mouse, and comparisons with the rat. Vision Res 25:21-31.
44. Schmidt TM, Kofuji P (2009) Functional and morphological differences among intrinsically photosensitive retinal ganglion cells. J Neurosci 29:476-482.
45. Schmidt TM, Kofuji P (2010) Differential cone pathway influence on intrinsically photosensitive retinal ganglion cell subtypes. J Neurosci 30:16262-16271.
46. Schmidt TM, Kofuji P (2011) Structure and function of bistratified intrinsically photosensitive retinal ganglion cells in the mouse. J Comp Neurol 519:1492-1504.
47. Schmidt TM, Taniguchi K, Kofuji P (2008) Intrinsic and extrinsic light responses in melanopsin-expressing ganglion cells during mouse development. J Neurophysiol 100:371-384.
48. Sun W, Li N, He S (2002) Large-scale morphological survey of mouse retinal ganglion cells. J Comp Neurol 451:115-126.
49. Van Hook MJ, Berson DM (2010) Hyperpolarization-activated current (I(h)) in ganglion-cell photoreceptors. PLoS One 5:e15344.
50. van Wyk M, Wässle H, Taylor WR (2009) Receptive field properties of ONand OFF-ganglion cells in the mouse retina. Vis Neurosci 26:297-308.
51. Viney TJ, Balint K, Hillier D, Siegert S, Boldogkoi Z, Enquist LW, Meister M, Cepko CL, Roska B (2007) Local retinal circuits of melanopsincontaining ganglion cells identified by transsynaptic viral tracing. Curr Biol 17:981-988.
52. Wang YV, Weick M, Demb JB (2011) Spectral and temporal sensitivity of cone-mediated responses in mouse retinal ganglion cells. J Neurosci 31:7670-7681.
53. Warren EJ, Allen CN, Brown RL, Robinson DW (2003) Intrinsic light responses of retinal ganglion cells projecting to the circadian system. Eur J Neurosci 17:1727-1735.
54. Wässle H, Puller C, Müller F, Haverkamp S (2009) Cone contacts, mosaics, and territories of bipolar cells in the mouse retina. J Neurosci 29:106-117.
55. Wong KY, Dunn FA, Berson DM (2005) Photoreceptor adaptation in intrinsically photosensitive retinal ganglion cells. Neuron 48:1001-1010.
56. Wong KY, Dunn FA, Graham DM, Berson DM (2007) Synaptic influences on rat ganglion-cell photoreceptors. J Physiol 582:279-296.
57. Zhang J, Li W, Hoshi H, Mills SL, Massey SC (2005) Stratification of alpha ganglion cells and ON/OFF directionally selective ganglion cells in the rabbit retina. Vis Neurosci 22:535-549.