Relationship between cholinergic amacrine cell and development of direction-selective ganglion cell dendritic field in mouse retina

doi:10.3877/cma.j.issn.2095-2007.2018.05.002

Abstract

Abstract:

Objective

To investigate the growth of retinal direction-selective ganglion cell’s dendritic field (DF) and it’s relationship with cholinergic amacrine mosaic.

Methods

Thirty six clean YFP (H) strains of transgenic mice were selected from the Laboratory Animal Center of Institute of Biophysics, Chinese Academy of Sciences. They were 0-1 month old, male and female.We compared the numbers of cholinergic amacrine cells within dendritic field of ON/OFF DSGC and OFF DGGC at several postnatal stages(P8, P13 and adulthood ) in mouse retina.

Results

As a classical directional selective ganglion cell, the dendrites of ON/OFF DSGC have two layers of dendritic structure. They are distributed in the ON and OFF sublayers of reticular layer in the retina. The angle between the curvature of the dendrites and the branches of the dendrites is relatively large. The branches return in the direction of the multidirectional cell bodies in a semi circular pattern. The prominent feature is the dendrites of the same cell. There will be no crossover. At P8, cholinergic amacrine cells in the DF range of D2 subclass ganglion cells contained (25.6±4.8) inner nuclear layers and (28.4±5.7) retinal ganglion cells respectively; at P13, cholinergic amacrine cells and (35.2±1.0) cholinergic amacrine cells in the DF range of D2 subclass ganglion cells contained (30.8±9.5) INL, respectively. (35.2±10.4) cholinergic amacrine cells of GCL; in adulthood, the DF range of D2 subclass ganglion cells contained (33.7±7.4) cholinergic amacrine cells of INL and (32.1±5.6) cholinergic amacrine cells of GCL, respectively. There was no significant difference in the number of cholinergic amacrine cells between the three periods (F=2.16, 1.55; P>0.05). In the DF range of OFF DSGC, the number of amacrine cells increased from P8 to P13, then decreased from P13 to adulthood. At P8, the number of amacrine cells in the DF range of GCL was (20.0±2.5), which was significantly less than that at P13 (32.0±7.1). In adulthood, the number decreased to (23.7±7.5). There was no significant difference in the number of cholinergic amacrine cells between the three periods (F=6.19, 1.55; P<0.05).

Conclusions

Our results indicated that ON/OFF DSGC achieved mature dendritic field size at very early postnatal stage which highly depended on cholinergic amacrine mosaic but was not influenced by bipolar cells input and light stimulation. While OFF DSGC likely involved different cellular and molecular mechanism.

Key words: Dendritic field(DF), Direction-selective ganglion cell(DSGC), Cholinergic amacrine cell

Lei Ren, Haitian Liang. Relationship between cholinergic amacrine cell and development of direction-selective ganglion cell dendritic field in mouse retina[J]. Chinese Journal of Ophthalmologic Medicine(Electronic Edition), 2018, 08(05): 202-208.

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References 53

[1]	Huxlin KR, Goodchild AK. Retinal ganglion cells in the albino rat: revised morphological classification[J]. J Comp Neurol, 1997, 385(2): 309-323.
[2]	Rockhill RL, Daly FJ, MacNeil MA, et al. The diversity of ganglion cells in a mammalian retina[J]. J Neurosci, 2002, 22(9): 3831-3843.
[3]	Sun W, Li N, He S. Large－scale morophological survey of rat retinal ganglion cells[J]. Vis Neurosci, 2002, 19(4): 483-493.
[4]	Baden T, Berens P, Franke K, et al. The functional diversity of retinal ganglion cells in the mouse[J]. Nature, 2016, 529(7586): 345-350.
[5]	Barlow CF. Clinical Aspects of the Blood－Brain Barrier[J]. Annual Review of Medicine, 1976, 2(6028): 133.
[6]	Fisher LJ. Development of retinal synaptic arrays in the inner plexiform layer of dark－reared mice[J]. J Embryol Exp Morphol, 1979, 54(Suppl 1): 219-227.
[7]	Rachel RA, Dolen G, Hayes NL, et al. Spatiotemporal features of early neuronogenesis differ in wild－type and albino mouse retina[J]. J Neurosci, 2002, 22(11): 4249-4263.
[8]	Galli－Resta L, Resta G, Tan SS, et al. Mosaics of islet－1－expressing amacrine cells assembled by short－range cellular interactions[J]. J Neurosci, 1997, 17(20): 7831-7838.
[9]	Zhang J, Yang Z, Wu SM. Development of cholinergic amacrine cells is visual activity－dependent in the postnatal mouse retina[J]. J Comp Neurol, 2005, 484(3): 331-343.
[10]	任蕾, 邸玉兰, 郑艳珍，等. 小鼠视网膜胆碱能无长突细胞阵列分布及发育过程中的变化[J]. 眼科新进展，2012，32(1)：1-4.
[11]	Kim IJ, Zhang Y, Yamagata M, et al. Molecular identification of a retinal cell type that responds to upward motion[J]. Nature, 2008, 452(7186): 478-482.
[12]	Diao L, Sun W, Deng Q, et al. Development of the mouse retina: emerging morphological diversity of the ganglion cells[J]. J Neurobiol, 2004, 61(2): 236-249.
[13]	Stacy RC, Wong RO. Developmental relationship between cholinergic amacrine cell processes and ganglion cell dendrites of the mouse retina[J]. J Comp Neurol, 2003, 456(2): 154-166.
[14]	Oyster CW, Barlow HB. Direction－selective units in rabbit retina: distribution of preferred directions[J]. Science, 1967, 155(3764): 841-842.
[15]	Sjöstrand FS.Movement perception, directionally selective ganglion cell responses and the involuntary eye movements. Neurophysiology at the level of information processing[J]．J Submicrosc Cytol Pathol, 2004, 36(1): 1-5.
[16]	Yonehara K, Ishikane H, Sakuta H, et al. Identification of retinal ganglion cells and their projections involved in central transmission of information about upward and downward image motion[J]. PLoS One, 2009, 4(1): e4320.
[17]	Yonehara K, Shintani T, Suzuki R, et al.Expression of SPIG1 reveals development of a retinal ganglion cell subtype projecting to the medial terminal nucleus in the mouse[J]．PLoS One, 2008, 3(2): e1533.
[18]	Famiglietti EV. Dendritic co－stratification of ON and ON－OFF directionally selective ganglion cells with starburst amacrine cells in rabbit retina[J]. J Comp Neurol, 1992, 324(3): 322-335.
[19]	Poznanski RR.Biophysical mechanisms and essential topography of directionally selective subunits in rabbit's retina[J]．J Integr Neurosci, 2005, 4(3): 341-361.
[20]	Borst A, Euler T. Seeing things in motion: models, circuits, and mechanisms[J]. Neuron, 2011, 71(6): 974-994.
[21]	Borst A．In search of the Holy Grail of fly motion vision[J]．Eur J Neurosci, 2014, 40(9): 3285-3293.
[22]	Massey SC, Linn DM, Kittila CA, et al. Contributions of GABAA receptors and GABAC receptors to acetylcholine release and directional selectivity in the rabbit retina[J]. Vis Neurosci, 1997, 14(5): 939-948.
[23]	Lukasiewicz PD, Eggers ED, Sagdullaev BT, et al.GABAC receptor－mediated inhibition in the retina[J]．Vision Res, 2004, 44(28): 3289-3296.
[24]	Yoshida K, Watanabe D, Ishikane H, et al. A key role of starburst amacrine cells in originating retinal directional selectivity and optokinetic eye movement[J]. Neuron, 2001, 30(3): 771-780.
[25]	Amthor FR, Keyser KT, Dmitrieva NA. Effects of the destruction of starburst－cholinergic amacrine cells by the toxin AF64A on rabbit retinal directional selectivity[J]. Vis Neurosci, 2002, 19(4): 495-509.
[26]	Famiglietti EV.Neural architecture of the " transient" ON directionally selective (class IIb1) ganglion cells in rabbit retina, partly co－stratified with starburst amacrine cells[J]．Vis Neurosci, 2016, 33: E004.
[27]	Vaney DI. 'Coronate' amacrine cells in the rabbit retina have the 'starburst' dendritic morphology[J]. Proc R Soc Lond B Biol Sci, 1984, 220(1221): 501-508.
[28]	Poznanski RR.Modelling the electrotonic structure of starburst amacrine cells in the rabbit retina: a functional interpretation of dendritic morphology[J]．Bull Math Biol, 1992, 54(6): 905-928.
[29]	Dong W, Sun W, Zhang Y, et al. Dendritic relationship between starburst amacrine cells and direction－selective ganglion cells in the rabbit retina[J]. J Physiol, 2004, 556(Pt 1): 11-7.
[30]	Chen YC, Chiao CC.Symmetric synaptic patterns between starburst amacrine cells and direction selective ganglion cells in the rabbit retina[J]．J Comp Neurol, 2008, 508(1): 175-183.
[31]	Euler T, Detwiler PB, Denk W. Directionally selective calcium signals in dendrites of starburst amacrine cells[J]. Nature, 2002, 418(6900): 845-852.
[32]	Hausselt SE, Euler T, Detwiler PB, et al.A dendrite－autonomous mechanism for direction selectivity in retinal starburst amacrine cells[J]．PLoS Biol, 2007, 5(7): e185.
[33]	Enciso GA, Rempe M, Dmitriev AV, et al. A model of direction selectivity in the starburst amacrine cell network[J]. J Comput Neurosci, 2010, 28(3): 567-578.
[34]	Poznanski RR.Cellular inhibitory behavior underlying the formation of retinal direction selectivity in the starburst network[J]．J Integr Neurosci, 2010, 9(3): 299-335.
[35]	Fried SI, Münch TA, Werblin FS.Mechanisms and circuitry underlying directional selectivity in the retina[J]．Nature, 2002, 420(6914): 411-414.
[36]	Taylor WR, Smith RG.The role of starburst amacrine cells in visual signal processing[J]．Vis Neurosci, 2012, 29(1): 73-81.
[37]	Wei W, Hamby AM, Zhou K, et al. Development of asymmetric inhibition underlying direction selectivity in the retina[J]. Nature, 2011, 469(7330): 402-406.
[38]	Park SJ, Kim IJ, Looger LL, et al.Excitatory synaptic inputs to mouse on－off direction－selective retinal ganglion cells lack direction tuning[J]．J Neurosci, 2014, 34(11): 3976-3981.
[39]	Dacheux RF, Chimento MF, Amthor FR. Synaptic input to the on－off directionally selective ganglion cell in the rabbit retina[J]. J Comp Neurol, 2003, 456(3): 267-278.
[40]	Famiglietti EV.Synaptic organization of complex ganglion cells in rabbit retina: type and arrangement of inputs to directionally selective and local－edge－detector cells[J]．J Comp Neurol, 2005 , 484(4): 357-391.
[41]	Briggman KL, Denk W. Towards neural circuit reconstruction with volume electron microscopy techniques[J]. Curr Opin Neurobiol, 2006, 16(5): 562-570.
[42]	Briggman KL, Bock DD.Volume electron microscopy for neuronal circuit reconstruction[J]．Curr Opin Neurobiol, 2012, 22(1): 154-161.
[43]	Morrie RD, Feller MB. An Asymmetric Increase in Inhibitory Synapse Number Underlies the Development of a Direction Selective Circuit in the Retina[J]. J Neurosci, 2015, 35(25): 9281-9286.
[44]	Pei Z, Chen Q, Koren D, et al.Conditional Knock－Out of Vesicular GABA Transporter Gene from Starburst Amacrine Cells Reveals the Contributions of Multiple Synaptic Mechanisms Underlying Direction Selectivity in the Retina[J]．J Neurosci, 2015, 35(38): 13219-13232.
[45]	Briggman KL, Helmstaedter M, Denk W. Wiring specificity in the direction－selectivity circuit of the retina[J]. Nature, 2011, 471(7337): 183-188.
[46]	Ding H, Smith RG, Poleg－Polsky A, et al.Species－specific wiring for direction selectivity in the mammalian retina[J]．Nature, 2016, 535(7610): 105-110.
[47]	Krishnaswamy A, Yamagata M, Duan X, et al. Sidekick 2 directs formation of a retinal circuit that detects differential motion[J]. Nature, 2015, 524(7566): 466-470.
[48]	Jacoby J, Schwartz GW.Three Small－Receptive－Field Ganglion Cells in the Mouse Retina Are Distinctly Tuned to Size, Speed, and Object Motion[J]．J Neurosci, 2017, 37(3): 610-625.
[49]	Yonehara K, Fiscella M, Drinnenberg A, et al. Congenital Nystagmus Gene FRMD7 Is Necessary for Establishing a Neuronal Circuit Asymmetry for Direction Selectivity[J]. Neuron, 2016, 89(1): 177-193.
[50]	Demb JB.Cellular mechanisms for direction selectivity in the retina[J]．Neuron, 2007, 55(2): 179-186.
[51]	Sivyer B, van Wyk M, Vaney DI, et al. Synaptic inputs and timing underlying the velocity tuning of direction－selective ganglion cells in rabbit retina[J]. J Physiol, 2010, 588(Pt 17): 3243-3253.
[52]	Vaney DI, Sivyer B, Taylor WR.Direction selectivity in the retina: symmetry and asymmetry in structure and function[J]．Nat Rev Neurosci, 2012, 13(3): 194-208.
[53]	Ackert JM, Farajian R, Volgyi B, et al. GABA blockade unmasks an OFF response in ON direction selective ganglion cells in the mammalian retina[J]. J Physiol, 2009, 587(Pt18): 4481-4495.

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