Photoresponse diversity among the five types of intrinsically photosensitive retinal ganglion cells
dc.contributor.author | Zhao, Xiwu | en_US |
dc.contributor.author | Stafford, Ben K. | en_US |
dc.contributor.author | Godin, Ashley L. | en_US |
dc.contributor.author | King, W. Michael | en_US |
dc.contributor.author | Wong, Kwoon Y. | en_US |
dc.date.accessioned | 2014-05-21T18:02:52Z | |
dc.date.available | WITHHELD_13_MONTHS | en_US |
dc.date.available | 2014-05-21T18:02:52Z | |
dc.date.issued | 2014-04-01 | en_US |
dc.identifier.citation | Zhao, Xiwu; Stafford, Ben K.; Godin, Ashley L.; King, W. Michael; Wong, Kwoon Y. (2014). "Photoresponse diversity among the five types of intrinsically photosensitive retinal ganglion cells." The Journal of Physiology 592(7): 1619-1636. | en_US |
dc.identifier.issn | 0022-3751 | en_US |
dc.identifier.issn | 1469-7793 | en_US |
dc.identifier.uri | https://hdl.handle.net/2027.42/106709 | |
dc.description.abstract | Intrinsically photosensitive retinal ganglion cells (ipRGCs) mediate non‐image‐forming visual responses, including pupillary constriction, circadian photoentrainment and suppression of pineal melatonin secretion. Five morphological types of ipRGCs, M1–M5, have been identified in mice. In order to understand their functions better, we studied the photoresponses of all five cell types, by whole‐cell recording from fluorescently labelled ipRGCs visualized using multiphoton microscopy. All ipRGC types generated melanopsin‐based (‘intrinsic’) as well as synaptically driven (‘extrinsic’) light responses. The intrinsic photoresponses of M1 cells were lower threshold, higher amplitude and faster than those of M2–M5. The peak amplitudes of extrinsic light responses differed among the ipRGC types; however, the responses of all cell types had comparable thresholds, kinetics and waveforms, and all cells received rod input. While all five types exhibited inhibitory amacrine‐cell and excitatory bipolar‐cell inputs from the ‘on’ channel, M1 and M3 received additional ‘off’‐channel inhibition, possibly through their ‘off’‐sublamina dendrites. The M2–M5 ipRGCs had centre–surround‐organized receptive fields, implicating a capacity to detect spatial contrast. In contrast, the receptive fields of M1 cells lacked surround antagonism, which might be caused by the surround of the inhibitory input nullifying the surround of the excitatory input. All ipRGCs responded robustly to a wide range of motion speeds, and M1–M4 cells appeared tuned to different speeds, suggesting that they might analyse the speed of motion. Retrograde labelling revealed that M1–M4 cells project to the superior colliculus, suggesting that the contrast and motion information signalled by these cells could be used by this sensorimotor area to detect novel objects and motion in the visual field. | en_US |
dc.publisher | Wiley Periodicals, Inc. | en_US |
dc.title | Photoresponse diversity among the five types of intrinsically photosensitive retinal ganglion cells | en_US |
dc.type | Article | en_US |
dc.rights.robots | IndexNoFollow | en_US |
dc.subject.hlbsecondlevel | Physiology | en_US |
dc.subject.hlbtoplevel | Health Sciences | en_US |
dc.description.peerreviewed | Peer Reviewed | en_US |
dc.description.bitstreamurl | http://deepblue.lib.umich.edu/bitstream/2027.42/106709/1/tjp6045.pdf | |
dc.description.bitstreamurl | http://deepblue.lib.umich.edu/bitstream/2027.42/106709/2/tjp6045-sup-0001-SuppMat.pdf | |
dc.identifier.doi | 10.1113/jphysiol.2013.262782 | en_US |
dc.identifier.source | The Journal of Physiology | en_US |
dc.identifier.citedreference | Schmidt TM & Kofuji P ( 2011 ). Structure and function of bistratified intrinsically photosensitive retinal ganglion cells in the mouse. J Comp Neurol 519, 1492 – 1504. | en_US |
dc.identifier.citedreference | Rodieck RW ( 1965 ). Quantitative analysis of cat retinal ganglion cell response to visual stimuli. Vision Res 5, 583 – 601. | en_US |
dc.identifier.citedreference | Schmidt TM & Kofuji P ( 2009 ). Functional and morphological differences among intrinsically photosensitive retinal ganglion cells. J Neurosci 29, 476 – 482. | en_US |
dc.identifier.citedreference | Schmidt TM & Kofuji P ( 2010 ). Differential cone pathway influence on intrinsically photosensitive retinal ganglion cell subtypes. J Neurosci 30, 16262 – 16271. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | Sexton TJ, Golczak M, Palczewski K & Van Gelder RN ( 2012 ). Melanopsin is highly resistant to light and chemical bleaching in vivo. J Biol Chem 287, 20888 – 20897. | en_US |
dc.identifier.citedreference | Trejo LJ & Cicerone CM ( 1984 ). Cells in the pretectal olivary nucleus are in the pathway for the direct light reflex of the pupil in the rat. Brain Res 300, 49 – 62. | en_US |
dc.identifier.citedreference | Tu DC, Zhang D, Demas J, Slutsky EB, Provencio I, Holy TE & Van Gelder RN ( 2005 ). Physiologic diversity and development of intrinsically photosensitive retinal ganglion cells. Neuron 48, 987 – 999. | en_US |
dc.identifier.citedreference | Van Hook MJ, Wong KY & Berson DM ( 2012 ). Dopaminergic modulation of ganglion‐cell photoreceptors in rat. Eur J Neurosci 35, 507 – 518. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | Waleszczyk WJ, Wang C, Burke W & Dreher B ( 1999 ). Velocity response profiles of collicular neurons: parallel and convergent visual information channels. Neuroscience 93, 1063 – 1076. | en_US |
dc.identifier.citedreference | Wang C, Waleszczyk WJ, Benedek G, Burke W & Dreher B ( 2001 ). Convergence of Y and non‐Y channels onto single neurons in the superior colliculi of the cat. Neuroreport 12, 2927 – 2933. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | Wei W, Elstrott J & Feller MB ( 2010 ). Two‐photon targeted recording of GFP‐expressing neurons for light responses and live‐cell imaging in the mouse retina. Nat Protoc 5, 1347 – 1352. | en_US |
dc.identifier.citedreference | Weng S, Estevez ME & Berson DM ( 2013 ). Mouse ganglion‐cell photoreceptors are driven by the most sensitive rod pathway and by both types of cones. PLoS One 8, e66480. | en_US |
dc.identifier.citedreference | Wong KY ( 2012 ). A retinal ganglion cell that can signal irradiance continuously for 10 hours. J Neurosci 32, 11478 – 11485. | en_US |
dc.identifier.citedreference | Wong KY, Dunn FA & Berson DM ( 2005 ). Photoreceptor adaptation in intrinsically photosensitive retinal ganglion cells. Neuron 48, 1001 – 1010. | en_US |
dc.identifier.citedreference | Wong KY, Dunn FA, Graham DM & Berson DM ( 2007 ). Synaptic influences on rat ganglion‐cell photoreceptors. J Physiol 582, 279 – 296. | en_US |
dc.identifier.citedreference | Aggelopoulos NC & Meissl H ( 2000 ). Responses of neurones of the rat suprachiasmatic nucleus to retinal illumination under photopic and scotopic conditions. J Physiol 523, 211 – 222. | en_US |
dc.identifier.citedreference | Allen AE, Brown TM & Lucas RJ ( 2011 ). A distinct contribution of short‐wavelength‐sensitive cones to light‐evoked activity in the mouse pretectal olivary nucleus. J Neurosci 31, 16833 – 16843. | en_US |
dc.identifier.citedreference | Altimus CM, Güler AD, Alam NM, Arman AC, Prusky GT, Sampath AP & Hattar S ( 2010 ). Rod photoreceptors drive circadian photoentrainment across a wide range of light intensities. Nat Neurosci 13, 1107 – 1112. | en_US |
dc.identifier.citedreference | Barlow HB, Hill RM & Levick WR ( 1964 ). Retinal Ganglion cells responding selectively to direction and speed of image motion in the rabbit. J Physiol 173, 377 – 407. | en_US |
dc.identifier.citedreference | Baver SB, Pickard GE & Sollars PJ ( 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. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | Berson DM, Dunn FA & Takao M ( 2002 ). Phototransduction by retinal ganglion cells that set the circadian clock. Science 295, 1070 – 1073. | en_US |
dc.identifier.citedreference | Brainard DH ( 1997 ). The Psychophysics Toolbox. Spat Vis 10, 433 – 436. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | Butler MP & Silver R ( 2011 ). Divergent photic thresholds in the non‐image‐forming visual system: entrainment, masking and pupillary light reflex. Proc Biol Sci 278, 745 – 750. | en_US |
dc.identifier.citedreference | Calvert PD, Krasnoperova NV, Lyubarsky AL, Isayama T, Nicoló M, Kosaras B, Wong G, Gannon KS, Margolskee RF, Sidman RL, Pugh EN Jr, Makino CL & Lem J ( 2000 ). Phototransduction in transgenic mice after targeted deletion of the rod transducin α‐subunit. Proc Natl Acad Sci U S A 97, 13913 – 13918. | en_US |
dc.identifier.citedreference | Chang B, Dacey MS, Hawes NL, Hitchcock PF, Milam AH, Atmaca‐Sonmez P, Nusinowitz S & Heckenlively JR ( 2006 ). Cone photoreceptor function loss‐3, a novel mouse model of achromatopsia due to a mutation in Gnat2. Invest Ophthalmol Vis Sci 47, 5017 – 5021. | en_US |
dc.identifier.citedreference | Clarke RJ, Zhang H & Gamlin PD ( 2003 ). Primate pupillary light reflex: receptive field characteristics of pretectal luminance neurons. J Neurophysiol 89, 3168 – 3178. | en_US |
dc.identifier.citedreference | Cohen HI, Winters RW & Hamasaki DI ( 1980 ). Response of X and Y cat retinal ganglion cells to moving stimuli. Exp Brain Res 38, 299 – 303. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | Einevoll GT & Plesser HE ( 2005 ). Response of the difference‐of‐Gaussians model to circular drifting‐grating patches. Vis Neurosci 22, 437 – 446. | en_US |
dc.identifier.citedreference | Estevez ME, Fogerson PM, Ilardi MC, Borghuis BG, Chan E, Weng S, Auferkorte ON, Demb JB & Berson DM ( 2012 ). Form and function of the M4 cell, an intrinsically photosensitive retinal ganglion cell type contributing to geniculocortical vision. J Neurosci 32, 13608 – 13620. | en_US |
dc.identifier.citedreference | Euler T, Hausselt SE, Margolis DJ, Breuninger T, Castell X, Detwiler PB & Denk W ( 2009 ). Eyecup scope—optical recordings of light stimulus‐evoked fluorescence signals in the retina. Pflugers Arch 457, 1393 – 1414. | en_US |
dc.identifier.citedreference | Frechette ES, Sher A, Grivich MI, Petrusca D, Litke AM & Chichilnisky EJ ( 2005 ). Fidelity of the ensemble code for visual motion in primate retina. J Neurophysiol 94, 119 – 135. | en_US |
dc.identifier.citedreference | Galindo‐Romero C, Jiménez‐López M, García‐Ayuso D, Salinas‐Navarro M, Nadal‐Nicolás FM, Agudo‐Barriuso M, Villegas‐Pérez MP, Avilés‐Trigueros M & Vidal‐Sanz M ( 2013 ). Number and spatial distribution of intrinsically photosensitive retinal ganglion cells in the adult albino rat. Exp Eye Res 108, 84 – 93. | en_US |
dc.identifier.citedreference | Groos GA & Mason R ( 1980 ). The visual properties of rat and cat suprachiasmatic neurones. J Comp Physiol 135, 349 – 356. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | Hattar S, Lucas RJ, Mrosovsky N, Thompson S, Douglas RH, Hankins MW, Lem J, Biel M, Hofmann F, Foster RG & Yau KW ( 2003 ). Melanopsin and rod–cone photoreceptive systems account for all major accessory visual functions in mice. Nature 424, 76 – 81. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | Hu C, Hill DD & Wong KY ( 2013 ). Intrinsic physiological properties of the five types of mouse ganglion‐cell photoreceptors. J Neurophysiol 109, 1876 – 1889. | en_US |
dc.identifier.citedreference | Lee BB & Willshaw DJ ( 1978 ). Responses of the various types of cat retinal ganglion cells to moving contours. Vision Res 18, 757 – 765. | en_US |
dc.identifier.citedreference | Lee HS, Nelms JL, Nguyen M, Silver R & Lehman MN ( 2003 ). The eye is necessary for a circadian rhythm in the suprachiasmatic nucleus. Nat Neurosci 6, 111 – 112. | en_US |
dc.identifier.citedreference | Lucas RJ, Hattar S, Takao M, Berson DM, Foster RG & Yau KW ( 2003 ). Diminished pupillary light reflex at high irradiances in melanopsin‐knockout mice. Science 299, 245 – 247. | en_US |
dc.identifier.citedreference | Neumann S, Haverkamp S & Auferkorte ON ( 2011 ). Intrinsically photosensitive ganglion cells of the primate retina express distinct combinations of inhibitory neurotransmitter receptors. Neuroscience 199, 24 – 31. | en_US |
dc.identifier.citedreference | Pu M ( 2000 ). Physiological response properties of cat retinal ganglion cells projecting to suprachiasmatic nucleus. J Biol Rhythms 15, 31 – 36. | en_US |
dc.owningcollname | Interdisciplinary and Peer-Reviewed |
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