GABA a receptors containing the α2 subunit are critical for direction-selective inhibition in the retina

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Auferkorte, Olivia Nicola ^a   Baden, Tom ^b   Kaushalya, Sanjeev Kumar ^c   Zabouri, Nawal ^a   Rudolph, Uwe ^d,e   Haverkamp, Silke ^a   Euler, Thomas ^b,f  

^a MAX PLANCK INSTITUTE FOR BRAIN RESEARCH   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c MAX PLANCK INSTITUTE FOR MEDICAL RESEARCH   (Germany)

^d MCLEAN HOSPITAL   (United States)

^e HARVARD MEDICAL SCHOOL   (United States)

^f UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR ALPHA2; 4 AMINOBUTYRIC ACID A RECEPTOR; GABRA2 PROTEIN, MOUSE;

ANIMAL TISSUE; ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DENDRITE; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; PROTEIN AGGREGATION; PROTEIN LOCALIZATION; RABBIT; RETINA; RETINA GANGLION CELL; RETINA INNER PLEXIFORM LAYER; SYNAPSE; ANIMAL; C57BL MOUSE; METABOLISM; MOUSE MUTANT; MOVEMENT PERCEPTION; PHOTOSTIMULATION; PHYSIOLOGY; RETINA AMACRINE CELL; SYNAPTOSOME;

MUS; ORYCTOLAGUS CUNICULUS;

AMACRINE CELLS; ANIMALS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MOTION PERCEPTION; PHOTIC STIMULATION; PRESYNAPTIC TERMINALS; RABBITS; RECEPTORS, GABA-A; RETINA; RETINAL GANGLION CELLS; SYNAPSES;

EID: 84859571931     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0035109     Document Type: Article

References (81)

1. Barlow HB, Hill RM, (1963) Selective sensitivity to direction of movement in ganglion cells of the rabbit retina. Science 139: 412-414.
2. 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.
3. Amthor FR, Oyster CW, Takahashi ES, (1984) Morphology of on-off direction-selective ganglion cells in the rabbit retina. Brain Res 298: 187-190.
4. Amthor FR, Takahashi ES, Oyster CW, (1989) Morphologies of rabbit retinal ganglion cells with complex receptive fields. J Comp Neurol 280: 97-121.
5. Oyster CW, Barlow HB, (1967) Direction-selective units in rabbit retina: distribution of preferred directions. Science 155: 841-842.
6. Oyster CW, Simpson JI, Takahashi ES, Soodak RE, (1980) Retinal ganglion cells projecting to the rabbit accessory optic system. J Comp Neurol 190: 49-61.
7. Buhl EH, Peichl L, (1986) Morphology of rabbit retinal ganglion cells projecting to the medial terminal nucleus of the accessory optic system. J Comp Neurol 253: 163-174.
8. Grzywacz NM, Amthor FR, (2007) Robust directional computation in on-off directionally selective ganglion cells of rabbit retina. Vis Neurosci 24: 647-661.
9. Kanjhan R, Sivyer B, (2010) Two types of ON direction-selective ganglion cells in rabbit retina. Neurosci Lett 483: 105-109.
10. Hoshi H, Tian LM, Massey SC, Mills SL, (2011) Two distinct types of ON directionally-selective ganglion cells in the rabbit retina. J Comp Neurol 519: 2509-2521.
11. Rivlin-Etzion M, Zhou K, Wei W, Elstrott J, Nguyen PL, et al. (2011) Transgenic mice reveal unexpected diversity of on-off direction-selective retinal ganglion cell subtypes and brain structures involved in motion processing. J Neurosci 31: 8760-8769.
12. Yonehara K, Ishikane H, Sakuta H, Shintani T, Nakamura-Yonehara K, et al. (2009) Identification of retinal ganglion cells and their projections involved in central transmission of information about upward and downward image motion. PLoS One 4: e4320.
13. Kay JN, De la Huerta I, Kim IJ, Zhang Y, Yamagata M, et al. (2011) Retinal ganglion cells with distinct directional preferences differ in molecular identity, structure, and central projections. J Neurosci 31: 7753-7762.
14. Kim IJ, Zhang Y, Yamagata M, Meister M, Sanes JR, (2008) Molecular identification of a retinal cell type that responds to upward motion. Nature 452: 478-482.
15. Trenholm S, Johnson K, Li X, Smith RG, Awatramani GB, (2011) Parallel mechanisms encode direction in the retina. Neuron 71: 683-694.
16. Hausselt SE, Euler T, (2008) Starburst Amacrine Cells and Direction Selectivity. In: Binder MD, Hirokawa N, Windhorst U, editors. Encyclopedia of Neuroscience Berlin, Heidelberg Springer pp. 3501-3507.
17. Masland RH, (2005) The many roles of starburst amacrine cells. Trends Neurosci 28: 395-396.
18. Demb JB, (2007) Cellular mechanisms for direction selectivity in the retina. Neuron 55: 179-186.
19. Euler T, Detwiler PB, Denk W, (2002) Directionally selective calcium signals in dendrites of starburst amacrine cells. Nature 418: 845-852.
20. Lee S, Zhou ZJ, (2006) The synaptic mechanism of direction selectivity in distal processes of starburst amacrine cells. Neuron 51: 787-799.
21. Hausselt SE, Euler T, Detwiler PB, Denk W, (2007) A dendrite-autonomous mechanism for direction selectivity in retinal starburst amacrine cells. PLoS Biol 5: e185.
22. Euler T, Hausselt SE, (2008) Direction Selective Cells. In: Masland RH, Albright TD, editors. The Senses- A Comprehensive Reference San Diego Academic Press pp. 413-422.
23. Gollisch T, Meister M, (2010) Eye smarter than scientists believed: neural computations in circuits of the retina. Neuron 65: 150-164.
24. Borst A, Haag J, Reiff DF, (2010) Fly motion vision. Annu Rev Neurosci 33: 49-70.
25. Borst A, Euler T, (2011) Seeing things in motion: models, circuits, and mechanisms. Neuron 71: 974-994.
26. Briggman KL, Euler T, (2011) Bulk electroporation and population calcium imaging in the adult mammalian retina. J Neurophysiol 105: 2601-2609.
27. Wei W, Hamby AM, Zhou K, Feller MB, (2011) Development of asymmetric inhibition underlying direction selectivity in the retina. Nature 469: 402-406.
28. Yonehara K, Balint K, Noda M, Nagel G, Bamberg E, et al. (2011) Spatially asymmetric reorganization of inhibition establishes a motion-sensitive circuit. Nature 469: 407-410.
29. Wyatt HJ, Daw NW, (1976) Specific effects of neurotransmitter antagonists on ganglion cells in rabbit retina. Science 191: 204-205.
30. Caldwell JH, Daw NW, Wyatt HJ, (1978) Effects of picrotoxin and strychnine on rabbit retinal ganglion cells: lateral interactions for cells with more complex receptive fields. J Physiol 276: 277-298.
31. Kittila CA, Massey SC, (1997) Pharmacology of directionally selective ganglion cells in the rabbit retina. J Neurophysiol 77: 675-689.
32. Massey SC, Linn DM, Kittila CA, Mirza W, (1997) Contributions of GABAA receptors and GABAC receptors to acetylcholine release and directional selectivity in the rabbit retina. Visual Neurosci 14: 939-948.
33. Yoshida K, Watanabe D, Ishikane H, Tachibana M, Pastan I, et al. (2001) A key role of starburst amacrine cells in originating retinal directional selectivity and optokinetic eye movement. Neuron 30: 771-780.
34. Amthor FR, Keyser KT, Dmitrieva NA, (2002) Effects of the destruction of starburst-cholinergic amacrine cells by the toxin AF64A on rabbit retinal directional selectivity. Visual Neurosci 19: 495-509.
35. Famiglietti EV, (1992) Dendritic co-stratification of ON and ON-OFF directionally selective ganglion cells with starburst amacrine cells in rabbit retina. J Comp Neurol 324: 322-335.
36. Jeon CJ, Kong JH, Strettoi E, Rockhill R, Stasheff SF, et al. (2002) Pattern of synaptic excitation and inhibition upon direction-selective retinal ganglion cells. J Comp Neurol 449: 195-205.
37. Chen YC, Chiao CC, (2008) Symmetric synaptic patterns between starburst amacrine cells and direction selective ganglion cells in the rabbit retina. J Comp Neurol 508: 175-183.
38. Denk W, Strickler JH, Webb WW, (1990) Two-photon laser scanning fluorescence microscopy. Science 248: 73-76.
39. Vollenweider I, Smith KS, Keist R, Rudolph U, (2011) Antidepressant-like properties of alpha2-containing GABA(A) receptors. Behav Brain Res 217: 77-80.
40. 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.
41. Greferath U, Grünert U, Fritschy JM, Stephenson A, Möhler H, et al. (1995) GABAA receptor subunits have differential distributions in the rat retina: in situ hybridization and immunohistochemistry. J Comp Neurol 353: 553-571.
42. Brandstätter JH, Koulen P, Wässle H, (1998) Diversity of glutamate receptors in the mammalian retina. Vision Res 38: 1385-1397.
43. Wässle H, Koulen P, Brandstätter JH, Fletcher EL, Becker CM, (1998) Glycine and GABA receptors in the mammalian retina. Vision Res 38: 1411-1430.
44. Kosaka T, Tauchi M, Dahl JL, (1988) Cholinergic neurons containing GABA-like and/or glutamic acid decarboxylase-like immunoreactivities in various brain regions of the rat. Exp Brain Res 70: 605-617.
45. Brecha N, Johnson D, Peichl L, Wässle H, (1988) Cholinergic amacrine cells of the rabbit retina contain glutamate decarboxylase and gamma-aminobutyrate immunoreactivity. Proc Natl Acad Sci U S A 85: 6187-6191.
46. Vaney DI, Young HM, (1988) GABA-like immunoreactivity in cholinergic amacrine cells of the rabbit retina. Brain Res 438: 369-373.
47. Briggman KL, Helmstädter M, Denk W, (2011) Wiring specificity in the direction-selectivity circuit of the retina. Nature 471: 183-188.
48. Vaney DI, (1990) The Mosaic of Amacrine Cells in the Mammalian Retina. Prog Retinal Res pp. 49-100.
49. Famiglietti EV, (1991) Synaptic organization of starburst amacrine cells in rabbit retina: analysis of serial thin sections by electron microscopy and graphic reconstruction. J Comp Neurol 309: 40-70.
50. Witschi R, Punnakkal P, Paul J, Walczak JS, Cervero F, et al. (2011) Presynaptic {alpha}2-GABAA Receptors in Primary Afferent Depolarization and Spinal Pain Control. J Neurosci 31: 8134-8142.
51. Borg-Graham LJ, (2001) The computation of directional selectivity in the retina occurs presynaptic to the ganglion cell. Nature Neurosci 4: 176-183.
52. Taylor WR, Vaney DI, (2002) Diverse synaptic mechanisms generate direction selectivity in the rabbit retina. J Neurosci 22: 7712-7720.
53. Fried SI, Münch TA, Werblin FS, (2002) Mechanisms and circuitry underlying directional selectivity in the retina. Nature 420: 411-414.
54. Fried SI, Münch TA, Werblin FS, (2005) Directional selectivity is formed at multiple levels by laterally offset inhibition in the rabbit retina. Neuron 46: 117-127.
55. Poleg-Polsky A, Diamond JS, (2011) Imperfect space clamp permits electrotonic interactions between inhibitory and excitatory synaptic conductances, distorting voltage clamp recordings. PLoS One 6: e19463.
56. Lee S, Kim K, Zhou ZJ, (2010) Role of ACh-GABA cotransmission in detecting image motion and motion direction. Neuron 68: 1159-1172.
57. Chen M, Weng S, Deng Q, Xu Z, He S, (2009) Physiological properties of direction-selective ganglion cells in early postnatal and adult mouse retina. J Physiol 587: 819-828.
58. Oesch NW, Taylor WR, (2010) Tetrodotoxin-resistant sodium channels contribute to directional responses in starburst amacrine cells. PLoS One 5: e12447.
59. Weng S, Sun W, He S, (2005) Identification of ON-OFF direction-selective ganglion cells in the mouse retina. J Physiol 562: 915-923.
60. Huberman AD, Wei W, Elstrott J, Stafford BK, Feller MB, et al. (2009) Genetic identification of an On-Off direction-selective retinal ganglion cell subtype reveals a layer-specific subcortical map of posterior motion. Neuron 62: 327-334.
61. Sun W, Li N, He S, (2002) Large-scale morphological survey of mouse retinal ganglion cells. J Comp Neurol 451: 115-126.
62. Badea TC, Nathans J, (2004) Quantitative analysis of neuronal morphologies in the mouse retina visualized by using a genetically directed reporter. J Comp Neurol 480: 331-351.
63. Kong JH, Fish DR, Rockhill RL, Masland RH, (2005) Diversity of ganglion cells in the mouse retina: unsupervised morphological classification and its limits. J Comp Neurol 489: 293-310.
64. 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.
65. Grzywacz NM, Sernagor E, (2000) Spontaneous activity in developing turtle retinal ganglion cells: statistical analysis. Visual Neurosci 17: 229-241.
66. Schachter MJ, Oesch N, Smith RG, Taylor WR, (2010) Dendritic spikes amplify the synaptic signal to enhance detection of motion in a simulation of the direction-selective ganglion cell. PLoS Computational Biol 6.
67. Fritschy JM, Brünig I, (2003) Formation and plasticity of GABAergic synapses: physiological mechanisms and pathophysiological implications. Pharmacol Ther 98: 299-323.
68. Nyíri G, Freund TF, Somogyi P, (2001) Input-dependent synaptic targeting of alpha(2)-subunit-containing GABA(A) receptors in synapses of hippocampal pyramidal cells of the rat. Eur J Neurosci 13: 428-442.
69. Brünig I, Scotti E, Sidler C, Fritschy JM, (2002) Intact sorting, targeting, and clustering of gamma-aminobutyric acid A receptor subtypes in hippocampal neurons in vitro. J Comp Neurol 443: 43-55.
70. Herd MB, Haythornthwaite AR, Rosahl TW, Wafford KA, Homanics GE, et al. (2008) The expression of GABAA beta subunit isoforms in synaptic and extrasynaptic receptor populations of mouse dentate gyrus granule cells. J Physiol 586: 989-1004.
71. Houston CM, Hosie AM, Smart TG, (2008) Distinct regulation of beta2 and beta3 subunit-containing cerebellar synaptic GABAA receptors by calcium/calmodulin-dependent protein kinase II. J Neurosci 28: 7574-7584.
72. Koulen P, (1999) Clustering of neurotransmitter receptors in the mammalian retina. J Membr Biol 171: 97-105.
73. Ghosh KK, Haverkamp S, Wässle H, (2001) Glutamate receptors in the rod pathway of the mammalian retina. J Neurosci 21: 8636-8647.
74. Zhang J, Diamond JS, (2009) Subunit- and pathway-specific localization of NMDA receptors and scaffolding proteins at ganglion cell synapses in rat retina. J Neurosci 29: 4274-4286.
75. Wässle H, Heinze L, Ivanova E, Majumdar S, Weiss J, et al. (2009) Glycinergic transmission in the Mammalian retina. Front Mol Neurosci 2: 6.
76. Zheleznova NN, Sedelnikova A, Weiss DS, (2009) Function and modulation of delta-containing GABA(A) receptors. Psychoneuroendocrinology 34 (Suppl 1): S67-73.
77. Euler T, Hausselt SE, Margolis DJ, Breuninger T, Castell X, et al. (2009) Eyecup scope-optical recordings of light stimulus-evoked fluorescence signals in the retina. Pflugers Arch 457: 1393-1414.
78. Panzanelli P, Bardy C, Nissant A, Pallotto M, Sassoe-Pognetto M, et al. (2009) Early synapse formation in developing interneurons of the adult olfactory bulb. J Neurosci 29: 15039-15052.
79. Dorostkar MM, Dreosti E, Odermatt B, Lagnado L, (2010) Computational processing of optical measurements of neuronal and synaptic activity in networks. J Neurosci Meth 188: 141-150.
80. Jeon CJ, Strettoi E, Masland RH, (1998) The major cell populations of the mouse retina. J Neurosci 18: 8936-8946.
81. 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.