Apoptosis Regulates IpRGC Spacing Necessary for Rods and Cones to Drive Circadian Photoentrainment

Overview

Journal Neuron

Publisher Cell Press

Specialty Neurology

Date 2013 Feb 12

PMID 23395376

Citations 27

Authors

Shih-Kuo Chen

Kylie S Chew

David S McNeill

Patrick W Keeley

Jennifer L Ecker

Buqing Q Mao

Johan Pahlberg

Bright Kim

Sammy C S Lee

Michael A Fox

William Guido

Kwoon Y Wong

Alapakkam P Sampath

Benjamin E Reese

Rejji Kuruvilla

Samer Hattar

Affiliations

Soon will be listed here.

Abstract

The retina consists of ordered arrays of individual types of neurons for processing vision. Here, we show that such order is necessary for intrinsically photosensitive retinal ganglion cells (ipRGCs) to function as irradiance detectors. We found that during development, ipRGCs undergo proximity-dependent Bax-mediated apoptosis. Bax mutant mice exhibit disrupted ipRGC spacing and dendritic stratification with an increase in abnormally localized synapses. ipRGCs are the sole conduit for light input to circadian photoentrainment, and either their melanopsin-based photosensitivity or ability to relay rod/cone input is sufficient for circadian photoentrainment. Remarkably, the disrupted ipRGC spacing does not affect melanopsin-based circadian photoentrainment but severely impairs rod/cone-driven photoentrainment. We demonstrate reduced rod/cone-driven cFos activation and electrophysiological responses in ipRGCs, suggesting that impaired synaptic input to ipRGCs underlies the photoentrainment deficits. Thus, for irradiance detection, developmental apoptosis is necessary for the spacing and connectivity of ipRGCs that underlie their functioning within a neural network.

Citing Articles

Retinal neurons establish mosaic patterning by excluding homotypic somata from their dendritic territories.

Kozlowski C, Hadyniak S, Kay J Cell Rep. 2024; 43(8):114615.

PMID: 39133615 PMC: 11440617. DOI: 10.1016/j.celrep.2024.114615.

Optimization-Based Pairwise Interaction Point Process (O-PIPP): A Precise and Universal Retinal Mosaic Modeling Approach.

He L, Wang W, Ma L, Huang T Invest Ophthalmol Vis Sci. 2024; 65(8):39.

PMID: 39042401 PMC: 11268446. DOI: 10.1167/iovs.65.8.39.

Retinal neurons establish mosaic patterning by excluding homotypic somata from their dendritic territory.

Kozlowski C, Hadyniak S, Kay J bioRxiv. 2023; .

PMID: 38014021 PMC: 10680827. DOI: 10.1101/2023.11.17.567616.

Retinal self-organization: a model of retinal ganglion cells and starburst amacrine cells mosaic formation.

de Montigny J, Sernagor E, Bauer R Open Biol. 2023; 13(4):220217.

PMID: 37015288 PMC: 10072945. DOI: 10.1098/rsob.220217.

Circuit mechanisms underlying embryonic retinal waves.

Voufo C, Chen A, Smith B, Yan R, Feller M, Tiriac A Elife. 2023; 12.

PMID: 36790167 PMC: 9988258. DOI: 10.7554/eLife.81983.

References

McNeill D, Sheely C, Ecker J, Badea T, Morhardt D, Guido W . Development of melanopsin-based irradiance detecting circuitry. Neural Dev. 2011; 6:8. PMC: 3070623. DOI: 10.1186/1749-8104-6-8. View

Hattar S, Kumar M, Park A, Tong P, Tung J, Yau K . Central projections of melanopsin-expressing retinal ganglion cells in the mouse. J Comp Neurol. 2006; 497(3):326-49. PMC: 2885916. DOI: 10.1002/cne.20970. View

Provencio I, Rollag M, Castrucci A . Photoreceptive net in the mammalian retina. This mesh of cells may explain how some blind mice can still tell day from night. Nature. 2002; 415(6871):493. DOI: 10.1038/415493a. View

Hattar S, Lucas R, Mrosovsky N, Thompson S, Douglas R, Hankins M . Melanopsin and rod-cone photoreceptive systems account for all major accessory visual functions in mice. Nature. 2003; 424(6944):76-81. PMC: 2885907. DOI: 10.1038/nature01761. View

COOK J, Chalupa L . Retinal mosaics: new insights into an old concept. Trends Neurosci. 2000; 23(1):26-34. DOI: 10.1016/s0166-2236(99)01487-3. View

Matsuoka R, Nguyen-Ba-Charvet K, Parray A, Badea T, Chedotal A, Kolodkin A . Transmembrane semaphorin signalling controls laminar stratification in the mammalian retina. Nature. 2011; 470(7333):259-63. PMC: 3063100. DOI: 10.1038/nature09675. View

Hirasawa H, Puopolo M, Raviola E . Extrasynaptic release of GABA by retinal dopaminergic neurons. J Neurophysiol. 2009; 102(1):146-58. PMC: 2712262. DOI: 10.1152/jn.00130.2009. View

Panda S, Sato T, Castrucci A, Rollag M, DeGrip W, Hogenesch J . Melanopsin (Opn4) requirement for normal light-induced circadian phase shifting. Science. 2002; 298(5601):2213-6. DOI: 10.1126/science.1076848. View

Zhang D, Wong K, Sollars P, Berson D, Pickard G, McMahon D . Intraretinal signaling by ganglion cell photoreceptors to dopaminergic amacrine neurons. Proc Natl Acad Sci U S A. 2008; 105(37):14181-6. PMC: 2544598. DOI: 10.1073/pnas.0803893105. View

10.

Berson D, Castrucci A, Provencio I . Morphology and mosaics of melanopsin-expressing retinal ganglion cell types in mice. J Comp Neurol. 2010; 518(13):2405-22. PMC: 2895505. DOI: 10.1002/cne.22381. View

11.

Takeuchi O, Fisher J, Suh H, Harada H, Malynn B, Korsmeyer S . Essential role of BAX,BAK in B cell homeostasis and prevention of autoimmune disease. Proc Natl Acad Sci U S A. 2005; 102(32):11272-7. PMC: 1183578. DOI: 10.1073/pnas.0504783102. View

12.

Wassle H . Parallel processing in the mammalian retina. Nat Rev Neurosci. 2004; 5(10):747-57. DOI: 10.1038/nrn1497. View

13.

Ecker J, Dumitrescu O, Wong K, Alam N, Chen S, LeGates T . Melanopsin-expressing retinal ganglion-cell photoreceptors: cellular diversity and role in pattern vision. Neuron. 2010; 67(1):49-60. PMC: 2904318. DOI: 10.1016/j.neuron.2010.05.023. View

14.

Freedman M, Lucas R, Soni B, von Schantz M, Munoz M, Foster R . Regulation of mammalian circadian behavior by non-rod, non-cone, ocular photoreceptors. Science. 1999; 284(5413):502-4. DOI: 10.1126/science.284.5413.502. View

15.

Guler A, Ecker J, Lall G, Haq S, Altimus C, Liao H . Melanopsin cells are the principal conduits for rod-cone input to non-image-forming vision. Nature. 2008; 453(7191):102-5. PMC: 2871301. DOI: 10.1038/nature06829. View

16.

Autret A, Martin S . Emerging role for members of the Bcl-2 family in mitochondrial morphogenesis. Mol Cell. 2009; 36(3):355-63. DOI: 10.1016/j.molcel.2009.10.011. View

17.

Hattar S, Liao H, Takao M, Berson D, Yau K . Melanopsin-containing retinal ganglion cells: architecture, projections, and intrinsic photosensitivity. Science. 2002; 295(5557):1065-70. PMC: 2885915. DOI: 10.1126/science.1069609. View

18.

Lucas R, Douglas R, Foster R . Characterization of an ocular photopigment capable of driving pupillary constriction in mice. Nat Neurosci. 2001; 4(6):621-6. DOI: 10.1038/88443. View

19.

Raven M, Eglen S, Ohab J, Reese B . Determinants of the exclusion zone in dopaminergic amacrine cell mosaics. J Comp Neurol. 2003; 461(1):123-36. DOI: 10.1002/cne.10693. View

20.

Lucas R, Hattar S, Takao M, Berson D, Foster R, Yau K . Diminished pupillary light reflex at high irradiances in melanopsin-knockout mice. Science. 2003; 299(5604):245-7. DOI: 10.1126/science.1077293. View