Spatial Relationships between GABAergic and Glutamatergic Synapses on the Dendrites of Distinct Types of Mouse Retinal Ganglion Cells across Development

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Bleckert, Adam ^a   Parker, Edward D ^b   Kang, YunHee ^c   Pancaroglu, Raika ^c   Soto, Florentina ^a   Lewis, Renate ^d   Craig, Ann Marie ^c   Wong, Rachel O L ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^d WASHINGTON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; CYAN FLUORESCENT PROTEIN; GLUTAMIC ACID; POSTSYNAPTIC DENSITY PROTEIN 95; YELLOW FLUORESCENT PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOLISTIC TRANSFORMATION; CELL TYPE; CONTROLLED STUDY; CORRELATION ANALYSIS; DENDRITE; GABAERGIC SYNAPSE; GLUTAMATERGIC SYNAPSE; ILLUMINATION; MOUSE; NONHUMAN; PERINATAL PERIOD; POSTSYNAPTIC MEMBRANE; PROTEIN EXPRESSION; RETINA; RETINA GANGLION CELL; SYNAPSE; SYNAPTOGENESIS; TRANSGENIC MOUSE;

AMACRINE CELLS; ANIMALS; ANTIGENS, THY-1; DENDRITES; EXCITATORY POSTSYNAPTIC POTENTIALS; FLUORESCENCE; GABAERGIC NEURONS; GLUTAMIC ACID; INHIBITORY POSTSYNAPTIC POTENTIALS; MICE; MICE, TRANSGENIC; RECEPTORS, GABA-A; RETINAL BIPOLAR CELLS; RETINAL GANGLION CELLS; STAINING AND LABELING; SYNAPSES;

EID: 84880778248     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0069612     Document Type: Article

References (91)

1. Jia H, Rochefort NL, Chen X, Konnerth A, (2010) Dendritic organization of sensory input to cortical neurons in vivo. Nature 464: 1307-1312.
2. Chen X, Leischner U, Rochefort NL, Nelken I, Konnerth A (2011) Functional mapping of single spines in cortical neurons in vivo. Nature.
3. Petreanu L, Mao T, Sternson SM, Svoboda K, (2009) The subcellular organization of neocortical excitatory connections. Nature 457: 1142-1145.
4. Bollmann JH, Engert F, (2009) Subcellular topography of visually driven dendritic activity in the vertebrate visual system. Neuron 61: 895-905.
5. Megias M, Emri ZS, Freund TF, Gulyas AI, (2001) Total number and distribution of inhibitory and excitatory synapses on hippocampal CA1 pyramidal cells. Neuroscience 102: 527-540.
6. Chen J, Villa K, Cha J, So P, Kubota Y, Nedivi E, (2012) Clustered Dynamics of Inhibitory Synapses and Dendritic Spines in the Adult Neocortex. Neuron 74: 361-373.
7. van Versendaal D, Rajendran R, Saiepour MH, Klooster J, Smit-Rigter L, et al. (2012) Elimination of inhibitory synapses is a major component of adult ocular dominance plasticity. Neuron 74: 374-383.
8. Gulyás AI, Megías M, Emri Z, Freund TF, (1999) Total number and ratio of excitatory and inhibitory synapses converging onto single interneurons of different types in the CA1 area of the rat hippocampus. J Neurosci 19: 10082-10097.
9. Masland RH, (2001) Neuronal diversity in the retina. Curr Opin Neurobiol 11: 431-436.
10. Sernagor E, Eglen SJ, Wong ROL, (2001) Development of retinal ganglion cell structure and function. Progress in Retinal and Eye Research 20: 139-174.
11. Sanes JR, Zipursky SL, (2010) Design principles of insect and vertebrate visual systems. Neuron 66: 15-36.
12. Sun W, Li N, He S, (2002) Large-scale morphological survey of mouse retinal ganglion cells. J Comp Neurol 451: 115-126.
13. Coombs JL, Van Der List D, Chalupa LM, (2007) Morphological properties of mouse retinal ganglion cells during postnatal development. J Comp Neurol 503: 803-814.
14. Völgyi B, Chheda S, Bloomfield SA, (2009) Tracer coupling patterns of the ganglion cell subtypes in the mouse retina. J Comp Neurol 512: 664-687.
15. Soto F, Bleckert A, Lewis R, Kang Y, Kerschensteiner D, et al. (2011) Coordinated increase in inhibitory and excitatory synapses onto retinal ganglion cells during development. Neural Dev 6: 31.
16. Varoqueaux F, Jamain S, Brose N, (2004) Neuroligin 2 is exclusively localized to inhibitory synapses. Eur J Cell Biol 83: 449-456.
17. Hoon M, Bauer G, Fritschy J-M, Moser T, Falkenburger BH, Varoqueaux F, (2009) Neuroligin 2 controls the maturation of GABAergic synapses and information processing in the retina. J Neurosci 29: 8039-8050.
18. Fisher LJ, (1979) Development of synaptic arrays in the inner plexiform layer of neonatal mouse retina. J Comp Neurol 187: 359-372.
19. He Q, Wang P, Tian N, (2011) Light-evoked synaptic activity of retinal ganglion and amacrine cells is regulated in developing mouse retina. Eur J Neurosci 33: 36-48.
20. 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.
21. Dobie FA, Craig AM, (2011) Inhibitory Synapse Dynamics: Coordinated Presynaptic and Postsynaptic Mobility and the Major Contribution of Recycled Vesicles to New Synapse Formation. J Neurosci 31: 10481-10493.
22. Feng G, Mellor RH, Bernstein M, Keller-Peck C, Nguyen QT, et al. (2000) Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28: 41-51.
23. Morgan JL, Kerschensteiner D, (2012) Coating gold particles with DNA (biolistics). Cold Spring Harb Protoc 2012: 114-117.
24. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, et al. (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9: 676-682.
25. Haverkamp S, Wässle H, (2000) Immunocytochemical analysis of the mouse retina. J Comp Neurol 424: 1-23.
26. Morgan JL, Schubert T, Wong ROL, (2008) Developmental patterning of glutamatergic synapses onto retinal ganglion cells. Neural Dev 3: 8.
27. Diao L, Sun W, Deng Q, He S, (2004) Development of the mouse retina: emerging morphological diversity of the ganglion cells. J Neurobiol 61: 236-249.
28. van Wyk M, Wässle H, Taylor WR, (2009) Receptive field properties of ON- and OFF-ganglion cells in the mouse retina. Vis Neurosci 26: 297-308.
29. Brandstätter JH, Greferath U, Euler T, Wässle H, (1995) Co-stratification of GABAA receptors with the directionally selective circuitry of the rat retina. Vis Neurosci 12: 345-358.
30. Auferkorte ON, Baden T, Kaushalya SK, Zabouri N, Rudolph U, et al. (2012) GABA(A) receptors containing the α2 subunit are critical for direction-selective inhibition in the retina. PLoS One 7: e35109.
31. SHOLL DA, (1953) Dendritic organization in the neurons of the visual and motor cortices of the cat. J Anat 87: 387-406.
32. Bishop D, Nikić I, Brinkoetter M, Knecht S, Potz S, et al. (2011) Near-infrared branding efficiently correlates light and electron microscopy. Nat Methods 8: 568-570.
33. Cardona A, Saalfeld S, Schindelin J, Arganda-Carreras I, Preibisch S, et al. (2012) TrakEM2 software for neural circuit reconstruction. PLoS One 7: e38011.
34. Dowling JE, Boycott BB, (1966) Organization of the primate retina: electron microscopy. Proc R Soc Lond B Biol Sci 166: 80-111.
35. Calkins DJ, Sterling P, (1996) Absence of spectrally specific lateral inputs to midget ganglion cells in primate retina. Nature 381: 613-615.
36. Kubota Y, Hatada SN, Kawaguchi Y, (2009) Important factors for the three-dimensional reconstruction of neuronal structures from serial ultrathin sections. Front Neural Circuits 3: 4.
37. Jeon CJ, Strettoi E, Masland RH, (1998) The major cell populations of the mouse retina. J Neurosci 18: 8936-8946.
38. Wick MJ, Radcliffe RA, Bowers BJ, Mascia MP, Lüscher B, et al. (2000) Behavioural changes produced by transgenic overexpression of gamma2L and gamma2S subunits of the GABAA receptor. Eur J Neurosci 12: 2634-2638.
39. Wu Y, Eghbali M, Ou J, Lu R, Toro L, Stefani E, (2010) Quantitative determination of spatial protein-protein correlations in fluorescence confocal microscopy. Biophys J 98: 493-504.
40. Jacob TC, Moss SJ, Jurd R, (2008) GABA(A) receptor trafficking and its role in the dynamic modulation of neuronal inhibition. Nat Rev Neurosci 9: 331-343.
41. Essrich C, Lorez M, Benson JA, Fritschy J-M, Luscher B, (1998) Postsynaptic clustering of major GABAA receptor subtypes requires the [gamma]2 subunit and gephyrin. Nat Neurosci 1: 563-571.
42. Sassoè-Pognetto M, Wässle H, (1997) Synaptogenesis in the rat retina: subcellular localization of glycine receptors, GABA(A) receptors, and the anchoring protein gephyrin. J Comp Neurol 381: 158-174.
43. Okabe S, Kim HD, Miwa A, Kuriu T, Okado H, (1999) Continual remodeling of postsynaptic density and its regulation by synaptic activity. Nat Neurosci 2: 804-811.
44. Sassoè-Pognetto M, Kirsch J, Grünert U, Greferath U, Fritschy JM, et al. (1995) Colocalization of gephyrin and GABAA-receptor subunits in the rat retina. J Comp Neurol 357: 1-14.
45. Zucker CL, (1998) Localization of gephyrin and glycine receptor subunit immunoreactivity in the rabbit retina. Vis Neurosci 15: 389-395.
46. Vithlani M, Terunuma M, Moss SJ, (2011) The dynamic modulation of GABA(A) receptor trafficking and its role in regulating the plasticity of inhibitory synapses. Physiol Rev 91: 1009-1022.
47. Greferath U, Grünert U, Fritschy JM, Stephenson A, Möhler H, Wässle H, (1995) GABAA receptor subunits have differential distributions in the rat retina: in situ hybridization and immunohistochemistry. J Comp Neurol 353: 553-571.
48. Xu Y, Vasudeva V, Vardi N, Sterling P, Freed MA, (2008) Different types of ganglion cell share a synaptic pattern. J Comp Neurol 507: 1871-1878.
49. Koizumi A, Jakobs TC, Masland RH, (2011) Regular mosaic of synaptic contacts among three retinal neurons. J Comp Neurol 519: 341-357.
50. Majumdar S, Heinze L, Haverkamp S, Ivanova E, Wässle H, (2007) Glycine receptors of A-type ganglion cells of the mouse retina. Vis Neurosci 24: 471-487.
51. Morgan JL, Soto F, Wong ROL, Kerschensteiner D, (2011) Development of cell type-specific connectivity patterns of converging excitatory axons in the retina. Neuron 71: 1014-1021.
52. Schwartz GW, Okawa H, Dunn FA, Morgan JL, Kerschensteiner D, et al. (2012) The spatial structure of a nonlinear receptive field. Nat Neurosci.
53. Chen X, Hsueh H-A, Greenberg K, Werblin FS, (2010) Three forms of spatial temporal feedforward inhibition are common to different ganglion cell types in rabbit retina. J Neurophysiol 103: 2618-2632.
54. Johnson J, Tian N, Caywood MS, Reimer RJ, Edwards RH, Copenhagen DR, (2003) Vesicular neurotransmitter transporter expression in developing postnatal rodent retina: GABA and glycine precede glutamate. J Neurosci 23: 518-529.
55. Unsoeld T, Stradomska AM, Wang R, Rathjen FG, Jüttner R, (2008) Early maturation of GABAergic synapses in mouse retinal ganglion cells. Int J Dev Neurosci 26: 233-238.
56. Benson DL, Cohen PA, (1996) Activity-independent segregation of excitatory and inhibitory synaptic terminals in cultured hippocampal neurons. J Neurosci 16: 6424-6432.
57. Zhao X, Shoji S, Lau P, (2005) Balanced GABAergic and glutamatergic synapse development in hippocampal neurons. Biochem Biophys Res Commun 330: 1110-1115.
58. Fried SI, Münch TA, Werblin FS, (2002) Mechanisms and circuitry underlying directional selectivity in the retina. Nature 420: 411-414.
59. Euler T, Detwiler PB, Denk W, (2002) Directionally selective calcium signals in dendrites of starburst amacrine cells. Nature 418: 845-852.
60. Weng S, Sun W, He S, (2005) Identification of ON-OFF direction-selective ganglion cells in the mouse retina. J Physiol 562: 915-923.
61. Taylor WR, Smith RG, (2012) The role of starburst amacrine cells in visual signal processing. Vis Neurosci 29: 73-81.
62. Wässle H, Boycott BB, (1991) Functional architecture of the mammalian retina. Physiol Rev 71: 447-480.
63. Tian N, Copenhagen DR, (2001) Visual deprivation alters development of synaptic function in inner retina after eye opening. Neuron 32: 439-449.
64. Wei W, Hamby AM, Zhou K, Feller MB, (2011) Development of asymmetric inhibition underlying direction selectivity in the retina. Nature 469: 402-406.
65. Klausberger T, Somogyi P, (2008) Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science 321: 53-57.
66. Jeon C-J, Kong J-H, Strettoi E, Rockhill R, Stasheff SF, Masland RH, (2002) Pattern of synaptic excitation and inhibition upon direction-selective retinal ganglion cells. J Comp Neurol 449: 195-205.
67. Briggman KL, Helmstaedter M, Denk W, (2011) Wiring specificity in the direction-selectivity circuit of the retina. Nature 471: 183-188.
68. Vaney DI, (1990) The mosaic of amacrine cells in the mammalian retina. Progress in retinal research 9: 49-100.
69. 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.
70. Jakobs TC, Koizumi A, Masland RH, (2008) The spatial distribution of glutamatergic inputs to dendrites of retinal ganglion cells. J Comp Neurol 510: 221-236.
71. Percival KA, Jusuf PR, Martin PR, Grünert U, (2009) Synaptic inputs onto small bistratified (blue-ON/yellow-OFF) ganglion cells in marmoset retina. J Comp Neurol 517: 655-669.
72. Percival KA, Martin PR, Grünert U, (2010) Synaptic inputs to two types of koniocellular pathway ganglion cells in marmoset retina. J Comp Neurol 519: 2135-2153.
73. Freed MA, Sterling P, (1988) The ON-alpha ganglion cell of the cat retina and its presynaptic cell types. J Neurosci 8: 2303-2320.
74. Cohen E, Sterling P, (1992) Parallel Circuits from Cones to the On-Beta Ganglion Cell. Eur J Neurosci 4: 506-520.
75. Kolb H, Nelson R, (1993) OFF-alpha and OFF-beta ganglion cells in cat retina: II. Neural circuitry as revealed by electron microscopy of HRP stains. J Comp Neurol 329: 85-110.
76. Owczarzak MT, Pourcho RG, (1999) Transmitter-specific input to OFF-alpha ganglion cells in the cat retina. Anat Rec 255: 363-373.
77. Freed MA, Smith RG, Sterling P, (1992) Computational model of the on-alpha ganglion cell receptive field based on bipolar cell circuitry. Proc Natl Acad Sci U S A 89: 236-240.
78. Tao HW, Zhang LI, Engert F, Poo M, (2001) Emergence of input specificity of ltp during development of retinotectal connections in vivo. Neuron 31: 569-580.
79. Harvey CD, Svoboda K, (2007) Locally dynamic synaptic learning rules in pyramidal neuron dendrites. Nature 450: 1195-1200.
80. Polsky A, Mel BW, Schiller J, (2004) Computational subunits in thin dendrites of pyramidal cells. Nat Neurosci 7: 621-627.
81. Yuste R, (2011) Dendritic spines and distributed circuits. Neuron 71: 772-781.
82. Sjöström PJ, Rancz EA, Roth A, Häusser M, (2008) Dendritic excitability and synaptic plasticity. Physiol Rev 88: 769-840.
83. Spolidoro M, Sale A, Berardi N, Maffei L, (2009) Plasticity in the adult brain: lessons from the visual system. Exp Brain Res 192: 335-341.
84. Liu G, (2004) Local structural balance and functional interaction of excitatory and inhibitory synapses in hippocampal dendrites. Nat Neurosci 7: 373-379.
85. Cafaro J, Rieke F, (2010) Noise correlations improve response fidelity and stimulus encoding. Nature 468: 964-967.
86. Nishimura Y, Rakic P, (1985) Development of the rhesus monkey retina. I. Emergence of the inner plexiform layer and its synapses. J Comp Neurol 241: 420-434.
87. Nishimura Y, Rakic P, (1987) Development of the rhesus monkey retina: II. A three-dimensional analysis of the sequences of synaptic combinations in the inner plexiform layer. J Comp Neurol 262: 290-313.
88. Vannier C, Triller A, (1997) Biology of the postsynaptic glycine receptor. Int Rev Cytol 176: 201-244.
89. Tretter V, Mukherjee J, Maric H-M, Schindelin H, Sieghart W, Moss SJ, (2012) Gephyrin, the enigmatic organizer at GABAergic synapses. Front Cell Neurosci 6: 23.
90. Koulen P, (1997) Vesicular acetylcholine transporter (VAChT): a cellular marker in rat retinal development. Neuroreport 8: 2845-2848.
91. Dong W, Sun W, Zhang Y, Chen X, He S, (2004) Dendritic relationship between starburst amacrine cells and direction-selective ganglion cells in the rabbit retina. J Physiol 556: 11-17.