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Synaptic Pattern of NMDA R1 upon the Direction-Selective Retinal Ganglion Cells in Developing Mouse Retina

발생 중 마우스 망막에서 방향특이성 신경절세포의 NMDA R1 수용체의 시냅스 패턴

  • Lee, Jee-Geon (Dept. of Biology, Kyungpook National University) ;
  • Kwon, Oh-Ju (Dept. of Optometry, Busan Institute of Science and Technology) ;
  • Jeon, Chang-Jin (Dept. of Biology, Kyungpook National University)
  • 이지건 (경북대학교 생명과학부 생물학과) ;
  • 권오주 (부산과학기술대학교 보건웰빙학부 안경광학과) ;
  • 전창진 (경북대학교 생명과학부 생물학과)
  • Received : 2013.10.30
  • Accepted : 2013.12.14
  • Published : 2013.12.31

Abstract

Purpose: To investigate the synaptic pattern of NMDA glutamate receptor subtype NMDA R1 on the dendritic arbors of ON-OFF direction-selective retinal ganglion cells (DS-RGSs) in developing [(5,10) days postnatal (PN)] mouse retina. Methods: ON-OFF DS-RGCs were injected with Lucifer yellow and the cells were identified by their characteristic morphology. To identify glutamatergic excitatory input from bipolar cell, we used a marker for the membrane traffic motor protein kinesin. Results: We identified DS-RGCs in P5, and P10 mouse retina. The immunofluorescence labeling of NMDA R1 was most prominent in the IPL. Our results showed that their presence upon the entire dendritic arbor of ON-OFF DS-RGCs is without any evidence of asymmetry, which would predict direction selectivity. Conclusions: The glutamatergic input from bipolar cell reveals symmetry pattern in all periods of P5, and P10. The results may suggest that direction selectivity not lies in the specific pattern of NMDA R1 receptors.

목적: 본 연구에서는 발생 중[태어난 지 5일(P5), 10일(P10)] 마우스 망막의 ON-OFF 방향특이성 신경절세포 수상돌기 상에서 NMDA R1 수용체의 시냅스 패턴을 연구하고자 하였다. 방법: ON-OFF 방향특이성 신경절세포는 Lucifer yellow를 주사하여 형태학적 특징으로 동정하였다. 이극세포로부터의 글루타메이트의 흥분성 유입을 확인하기 위해 membrane traffic motor 단백질 마커인 kinesin을 이용하였다. 결과: 본 연구에서 P5, P10의 ON-OFF 방향특이성 신경절세포를 동정할 수 있었으며, NMDA R1의 면역반응반점은 내망상층에서 강하게 나타났다. ON-OFF 방향특이성 신경절세포의 수상돌기상의 수용체의 분포패턴에서 방향특이성을 예측할 수 있는 어떠한 비대칭성도 발견하지 못하였다. 결론: 이극세포로부터의 글루타메이트성 자극유입은 P5, P10 단계에서 모두 균형적으로 유입되며, 방향특이성은 NMDA R1 수용체의 특이적인 패턴에 있지 않음을 밝혔다.

Keywords

References

  1. Masland RH. Neuronal cell types. Curr Biol. 2004; 14(13):497-500. https://doi.org/10.1016/j.cub.2004.06.035
  2. Taylor WR, Vaney DI. Diverse synaptic mechanisms generate direction selectivity in the rabbit retina. J Neurosci. 2002;22(17):7712-7720.
  3. Vaney DI, Sivyer B, Taylor WR. Direction selectivity in the retina: symmetry and asymmetry in structure and function. Nat Rev Neurosci. 2012;13(3):194-208.
  4. Barlow HB, Hill RM. Selective sensitivity to direction of movement in ganglion cells of the rabbit retina. Science. 1963;139(3553):412-414. https://doi.org/10.1126/science.139.3553.412
  5. Barlow HB, Levick WR. The mechanism of directionally selective units in rabbit's retina. J Physiol. 1965;178(3): 477-504. https://doi.org/10.1113/jphysiol.1965.sp007638
  6. Borg-Graham LJ. The computation of directional selectivity in the retina occurs presynaptic to the ganglion cell. Nat Neurosci. 2001;4(2):176-183. https://doi.org/10.1038/84007
  7. Briggman KL, Helmstaedter M, Denk W. Wiring specificity in the direction-selectivity circuit of the retina. Nature. 2011;471(7337):183-188. https://doi.org/10.1038/nature09818
  8. Koizumi A, Jakobs TC, Masland RH. Regular mosaic of synaptic contacts among three retinal neurons. J Comp Neurol. 2011;519(2):341-357. https://doi.org/10.1002/cne.22522
  9. Masland RH. The many roles of starburst amacrine cells. Trends Neurosci. 2005;28(8):395-396. https://doi.org/10.1016/j.tins.2005.06.002
  10. Taylor WR, He S, Levick WR, Vaney DI. Dendritic computation of direction selectivity by retinal ganglion cells. Science. 2000;289(5488):2347-2350. https://doi.org/10.1126/science.289.5488.2347
  11. Wei W, Hamby AM, Zhou K, Feller MB. Development of asymmetric inhibition underlying direction selectivity in the retina. Nature. 2011;469(7330):402-406. https://doi.org/10.1038/nature09600
  12. Yonehara K, Balint K, Noda M, Nagel G, Bamberg E, Roska B. Spatially asymmetric reorganization of inhibition establishes a motion-sensitive circuit. Nature. 2011; 469(7330):407-410. https://doi.org/10.1038/nature09711
  13. Yoshida K, Watanabe D, Ishikane H, Tachibana M, Pastan I, Nakanishi S. A key role of starburst amacrine cells in originating retinal directional selectivity and optokinetic eye movement. Neuron. 2001;30(3):771-780. https://doi.org/10.1016/S0896-6273(01)00316-6
  14. Weng S, Sun W, He S. Identification of ON-OFF directionselective ganglion cells in the mouse retina. J Physiol. 2005;562(3):915-923. https://doi.org/10.1113/jphysiol.2004.076695
  15. Sun W, Deng Q, Levick WR, He S. ON direction-selective ganglion cells in the mouse retina. J Physiol. 2006; 576(1):197-202. https://doi.org/10.1113/jphysiol.2006.115857
  16. Kim IJ, Zhang Y, Yamagata M, Meister M, Sanes JR. Molecular identification of a retinal cell type that responds to upward motion. Nature. 2008;452(7186):478-482. https://doi.org/10.1038/nature06739
  17. Ariel M, Daw NW. Pharmacological analysis of directionally sensitive rabbit retinal ganglion cells. J Physiol. 1982;324(1):161-185. https://doi.org/10.1113/jphysiol.1982.sp014105
  18. Amthor FR, Oyster CW, Takahashi ES. Morphology of on-off direction-selective ganglion cells in the rabbit retina. Brain Res. 1984;298(1):187-190. https://doi.org/10.1016/0006-8993(84)91167-3
  19. Sun W, Li N, He S. Largescale morphological survey of mouse retinal ganglion cells. J Comp Neurol. 2002; 451(2):115-126. https://doi.org/10.1002/cne.10323
  20. Vaney DI. Territorial organization of direction-selective ganglion cells in rabbit retina. J Neurosci. 1994;14(11): 6301-6316.
  21. Vaney DI, Taylor WR. Direction selectivity in the retina. Curr Opi Neurobiol. 2002;12(4):405-410. https://doi.org/10.1016/S0959-4388(02)00337-9
  22. Yonehara K, Farrow K, Ghanem A, Hillier D, Balint K, Teixeira M et al. The first stage of cardinal direction selectivity is localized to the dendrites of retinal ganglion cells. Neuron. 2013;79(6):1078-1085. https://doi.org/10.1016/j.neuron.2013.08.005
  23. Chan YC, Chiao CC. The distribution of the preferred directions of the ON-OFF direction selective ganglion cells in the rabbit retina requires refinement after eye opening. Physiol Rep. 2013;1(2):e00013.
  24. McLaughlin T, Torborg CL, Feller MB, O'Leary DD. Retinotopic map refinement requires spontaneous retinal waves during a brief critical period of development. Neuron. 2003;40(6):1147-1160. https://doi.org/10.1016/S0896-6273(03)00790-6
  25. Ames A, Nesbett FB. In vitro retina as an experimental model of the central nervous system. J Neurochem. 1981;37(4):867-877. https://doi.org/10.1111/j.1471-4159.1981.tb04473.x
  26. Yang G, Masland RH. Receptive fields and dendritic structure of directionally selective retinal ganglion cells. J Neurosci. 1994;14(9):5267-5280.
  27. Yang G, Masland RH. Direct visualization of the dendritic and receptive fields of directionally selective retinal ganglion cells. Science. 1992;258(5090):1949-1952. https://doi.org/10.1126/science.1470920
  28. Jeon CJ, Strettoi E, Masland RH. The major cell populations of the mouse retina. J Neurosci. 1998;18(21):8936- 8946.
  29. Jeon CJ, Kong JH, Strettoi E, Rockhill R, Stasheff SF, Masland RH. Pattern of synaptic excitation and inhibition upon directionselective retinal ganglion cells. J Comp Neurol. 2002;449(2):195-205. https://doi.org/10.1002/cne.10288
  30. Panno JP. Symmetry analysis of cell nuclei. Cytometry. 1988;9(3):195-200. https://doi.org/10.1002/cyto.990090302
  31. Haverkamp S, Wssle H. Immunocytochemical analysis of the mouse retina. J Comp Neurol. 2000;424(1):1-23. https://doi.org/10.1002/1096-9861(20000814)424:1<1::AID-CNE1>3.0.CO;2-V
  32. Watanabe M, Mishina M, Inoue Y. Differential distributions of the NMDA receptor channel subunit mRNAs in the mouse retina. Brain Res. 1994;634(2):328-332. https://doi.org/10.1016/0006-8993(94)91938-0
  33. Muresan V, Lyass A, Schnapp BJ. The kinesin motor KIF3A is a component of the presynaptic ribbon in vertebrate photoreceptors. J Neurosci. 1999;19(3):1027-1037.
  34. Bowe-Anders C, Miller RF, Dacheux R. Developmental characteristics of receptive organization in the isolated retina-eyecup of the rabbit. Brain Res. 1975;87(1):61-65. https://doi.org/10.1016/0006-8993(75)90779-9
  35. Masland RH. Maturation of function in the developing rabbit retina. J Comp Neurol. 1977;175(3):275-286. https://doi.org/10.1002/cne.901750303
  36. Chan YC, Chiao CC. Effect of visual experience on the maturation of ON-OFF direction selective ganglion cells in the rabbit retina. Vision Res. 2008;48(23-24):2466-2475. https://doi.org/10.1016/j.visres.2008.08.010
  37. Elstrott J, Anishchenko A, Greschner M, Sher A, Litke AM, Chichilnisky EJ, Feller MB. Direction selectivity in the retina is established independent of visual experience and cholinergic retinal waves. Neuron. 2008;58(4):499- 506. https://doi.org/10.1016/j.neuron.2008.03.013
  38. Sun L, Han X, He S. Direction-selective circuitry in rat retina develops independently of GABAergic, cholinergic and action potential activity. PLoS One. 2011;6(5):e19477. https://doi.org/10.1371/journal.pone.0019477
  39. Coombs JL, Van Der List D, Chalupa LM. Morphological properties of mouse retinal ganglion cells during postnatal development. J Comp Neurol. 2007;503(6):803-814. https://doi.org/10.1002/cne.21429
  40. Massey SC. Cell types using glutamate as a neurotransmitter in the vertebrate retina. Prog Ret Res. 1990;9:399- 425. https://doi.org/10.1016/0278-4327(90)90013-8
  41. Massey SC, Maguire G. The role of glutamate in retinal circuitry. In Excitatory Amino Acids and Synaptic Transmis sion, San Diego: Academic Press, 1995;201-221.
  42. Massey SC, Miller RF. N-methyl-D-aspartate receptors of ganglion cells in rabbit retina. J Neurophysiol. 1990;63(1):16- 30.
  43. Hollmann M, Heinemann S. Cloned glutamate receptors. Annu Rev Neurosci. 1994;17(1):31-108. https://doi.org/10.1146/annurev.ne.17.030194.000335
  44. Ozawa S, Kamiya H, Tsuzuki K. Glutamate receptors in the mammalian central nervous system. Prog Neurobiol. 1998;54(5):581-618. https://doi.org/10.1016/S0301-0082(97)00085-3
  45. Monaghan DT, Bridges RJ, Cotman CW. The excitatory amino acid receptors: their classes, pharmacology, and distinct properties in the function of the central nervous system. Annu Rev Pharmacol Toxicol. 1989;29(1):365- 402. https://doi.org/10.1146/annurev.pa.29.040189.002053
  46. Kittila CA, Massey SC. Pharmacology of directionally selective ganglion cells in the rabbit retina. J Neurophysiol. 1997;77(2):675-689.
  47. Tjepkes DS, Amthor FR. The role of NMDA channels in rabbit retinal directional selectivity. Vis Neurosci. 2000; 17(2):291-302.
  48. Cohen ED, Miller RF. Quinoxalines block the mechanism of directional selectivity in ganglion cells of the rabbit retina. Proc Natl Acad Sci. 1995;92(4):1127-1131. https://doi.org/10.1073/pnas.92.4.1127
  49. Lee JG, Lee KP, Jeon CJ. Synaptic pattern of KA1 and KA2 upon the direction-selective ganglion cells in developing and adult mouse retina. Acta Histochem Cytochem. 2012;45(1):35-45. https://doi.org/10.1267/ahc.11043
  50. Catalano SM, Chang CK, Shatz CJ. Activity-dependent regulation of NMDAR1 immunoreactivity in the developing visual cortex. J Neurosci. 1997;17(21):8376-8390.
  51. Guenther E, Schmid S, Wheeler-Schilling T, Albach G, Grnder T, Fauser S, Kohler K. Developmental plasticity of NMDA receptor function in the retina and the influence of light. FASEB J. 2004;18(12):1433-1435.
  52. Kirkwood A, Rioult MC, Bear MF. Experience-dependent modification of synaptic plasticity in visual cortex. Nature. 1996;381(6582):526-528. https://doi.org/10.1038/381526a0
  53. Xue J, Cooper NG. The modification of NMDA receptors by visual experience in the rat retina is age dependent. Brain Res Mol Brain Res. 2001;91(1-2):196-203. https://doi.org/10.1016/S0169-328X(01)00141-3
  54. Chang YC, Chen CY, Chiao CC. Visual experience-independent functional expression of NMDA receptors in the developing rabbit retina. IOVS. 2010;51(5):2744-2754.
  55. Lee S, Kim K, Zhou ZJ. Role of ACh-GABA cotransmission in detecting image motion and motion direction. Neuron. 2010;68(6):1159-1172. https://doi.org/10.1016/j.neuron.2010.11.031

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