GABAA receptor-mediated signaling alters the structure of spontaneous activity in the developing retina

Journal of Neuroscience

Volumn 27, Issue 34, 2007, Pages 9130-9140

  Wang, Chih Tien ^a,d   Blankenship, Aaron G ^a   Anishchenko, Anastasia ^a   Elstrott, Justin ^a   Fikhman, Michael ^a   Nakanishi, Shigetada ^b,c   Feller, Marla B ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b OSAKA BIOSCIENCE INSTITUTE   (Japan)

^c KYOTO UNIVERSITY   (Japan)

^d NATIONAL TAIWAN UNIVERSITY   (Taiwan)

Author keywords

Adenosine receptor; Aminophylline; Retinal ganglion cell; Retinal waves; Spontaneous activity; Starburst amacrine cell

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; ADENOSINE RECEPTOR; AMINOPHYLLINE;

4 AMINOBUTYRIC ACID RELEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; ELECTROPHYSIOLOGY; GABAERGIC SYSTEM; IMMUNOFLUORESCENCE; MEMBRANE DEPOLARIZATION; MOUSE; NERVE EXCITABILITY; NONHUMAN; PRIORITY JOURNAL; RECEPTOR BLOCKING; RETINA DEVELOPMENT; RETINA GANGLION CELL; SIGNAL TRANSDUCTION; SYNAPTIC INHIBITION;

AMACRINE CELLS; AMINOPHYLLINE; ANIMALS; ANIMALS, NEWBORN; DRUG INTERACTIONS; GABA AGENTS; GREEN FLUORESCENT PROTEINS; MEMBRANE POTENTIALS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PATCH-CLAMP TECHNIQUES; PHOSPHODIESTERASE INHIBITORS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA-A; RETINA; RETINAL GANGLION CELLS; VISUAL PATHWAYS;

EID: 34548179073     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1293-07.2007     Document Type: Article

References (80)

1. Bansal A, Singer J, Hwang B, Feller M (2000) Mice lacking specific nAChR subunits exhibit dramatically altered spontaneous activity patterns and reveal a limited role for retinal waves in forming ON/OFF circuits in the inner retina. J Neurosci 20:7672-7681.
2. Ben-Ari Y (2001) Developing networks play a similar melody. Trends Neurosci 24:353-360.
3. Ben-Ari Y (2002) Excitatory actions of gaba during development: the nature of the nurture. Nat Rev Neurosci 3:728-739.
4. Ben-Ari Y, Khalilov I, Represa A, Gozlan H (2004) Interneurons set the tune of developing networks. Trends Neurosci 27:422-427.
5. Berg RW, Alaburda A, Hounsgaard J (2007) Balanced inhibition and excitation drive spike activity in spinal half-centers. Science 315:390-393.
6. Brickley SG, Cull-Candy SG, Farrant M (1996) Development of a tonic form of synaptic inhibition in rat cerebellar granule cells resulting from persistent activation of GABAA receptors. J Physiol (Lond) 497:753-759.
7. Butts DA, Feller MB, Shatz CJ, Rokhsar DS (1999) Retinal waves are governed by collective network properties. J Neurosci 19:3580-3593.
8. B receptors regulate chick retinal calcium waves. J Neurosci 21:897-910.
9. Chadderton P, Margrie TW, Hausser M (2004) Integration of quanta in cerebellar granule cells during sensory processing. Nature 428:856-860.
10. Chance FS, Abbott LF, Reyes AD (2002) Gain modulation from background synaptic input. Neuron 35:773-782.
11. Clark BD, Newman EA (2005) Adenosine-evoked hyperpolarization of retinal ganglion cells is mediated by GIRK channel activation. Soc Neurosci Abstr 31:375.5.
12. Cobb SR, Buhl EH, Halasy K, Paulsen O, Somogyi P (1995) Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature 378:75-78.
13. Colicos M, Firth S, Bosze J, Goldstein J, Feller M (2004) Emergence of realistic retinal networks in culture promoted by the superior colliculus. Dev Neurosci 26:406-416.
14. A receptor-mediated tonic inhibition in thalamic neurons. J Neurosci 25:11553-11563.
15. Davies LP, Hambley JW, Johnston GA (1982) Ethylenediamine as a GABA agonist: enhancement of diazepam binding and interaction with GABA receptors and uptake sites. Neurosci Lett 29:57- 61.
16. De Koninck Y, Mody I (1994) Noise analysis of miniature IPSCs in adult rat brain slices: properties and modulation of synaptic GABAA receptor channels. J Neurophysiol 71:1318-1335.
17. Demarque M, Represa A, Becq H, Khalilov I, Ben-Ari Y, Aniksztejn L (2002) Paracrine intercellular communication by a Ca2+- and SNARE-independent release of GABA and glutamate prior to synapse formation. Neuron 36:1051-1061.
18. Farrant M, Nusser Z (2005) Variations on an inhibitory theme: phasic and tonic activation of GABA(A) receptors. Nat Rev Neurosci 6:215-229.
19. Feller MB, Wellis DP, Stellwagen D, Werblin FS, Shatz CJ (1996) Requirement for cholinergic synaptic transmission in the propagation of spontaneous retinal waves. Science 272:1182-1187.
20. Fischer K, Lukasiewicz P, Wong R (1998) Age-dependent and cell-class specific modulation of retinal ganglion cell bursting activity by GABA. J Neurosci 18:3767-3778.
21. Garaschuk O, Hanse E, Konnerth A (1998) Developmental profile and synaptic origin of early network oscillations in the CA1 region of rat neonatal hippocampus. J Physiol (Lond) 507:219-236.
22. Greferath U, Grunert U, Mohler H, Wassle H (1993) Cholinergic amacrine cells of the rat retina express the delta-subunit of the GABAA-receptor. Neurosci Lett 163:71-73.
23. Grunert U (1999) Distribution of GABAA and glycine receptors in the mammalian retina. Clin Exp Pharmacol Physiol 26:941-944.
24. Gulati K, Ray A, Pal G, Vijayan VK (2005) Possible role of free radicals in theophylline-induced seizures in mice. Pharmacol Biochem Behav 82:241-245.
25. Hensch TK, Fagiolini M (2005) Excitatory-inhibitory balance and critical period plasticity in developing visual cortex. Prog Brain Res 147:115-124.
26. Huberman AD (2007) Mechanisms of eye-specific visual circuit development. Curr Opin Neurobiol 17:73-80.
27. Jensen K, Chiu CS, Sokolova I, Lester HA, Mody I (2003) GABA transporter-1 (GAT1)-deficient mice: differential tonic activation of GABAA versus GABAB receptors in the hippocampus. J Neurophysiol 90:2690-2701.
28. 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.
29. Kaneda M, Farrant M, Cull-Candy SG (1995) Whole-cell and singlechannel currents activated by GABA and glycine in granule cells of the rat cerebellum. J Physiol (Lond) 485:419-435.
30. Lee CW, Eglen SJ, Wong RO (2002) Segregation of ON and OFF retinogeniculate connectivity directed by patterned spontaneous activity. J Neurophysiol 88:2311-2321.
31. Leinekugel X, Medina I, Khalilov I, Ben-Ari Y, Khazipov R (1997) Ca2+ oscillations mediated by the synergistic excitatory actions of GABA(A) and NMDA receptors in the neonatal hippocampus. Neuron 18:243-255.
32. Litke A, Bezayiff N, Chichilnisky E, Cunningham W, Dabrowski W, Grillo A, Grivich M, Grybos P, Hottowy P, Kachiguine S, Kalmar R, Mathieson K, Petrusca D, Rahman M, Sher A (2004) What does the eye tell the brain? Development of a system for the large-scale recording of retinal output activity. IEEE Trans Nucl Sci 51:1434-1440.
33. Litke AM, Chichilnisky EJ, Dabrowski W, Grillo AA, Grybos P, Kachiguine S, Rahman M, Taylor G (2003) Large-scale imaging of retinal output activity. Nucl Instrum Methods Phys Res A 501:298-307.
34. Liu Z, Neff RA, Berg DK (2006) Sequential interplay of nicotinic and GABAergic signaling guides neuronal development. Science 314:1610-1613.
35. Long MA, Cruikshank SJ, Jutras MJ, Connors BW (2005) Abrupt maturation of a spike-synchronizing mechanism in neocortex. J Neurosci 25:7309-7316.
36. Marchionni I, Omrani A, Cherubini E (2007) In the developing rat hippocampus a tonic GABAA-mediated conductance selectively enhances the glutamatergic drive of principal cells. J Physiol (Lond) 581:515-528.
37. McCartney MR, Deeb TZ, Henderson TN, Hales TG (2007) Tonically active GABAA receptors in hippocampal pyramidal neurons exhibit constitutive GABA-independent gating. Mol Pharmacol 71:539-548.
38. McLaughlin T, Torborg CL, Feller M, O'Leary DDM (2003) Retinotopic map refinement requires spontaneous retinal waves during a brief critical period of development. Neuron 40:1147-1160.
39. Medina AE, Krahe TE, Ramoa AS (2005) Early alcohol exposure induces persistent alteration of cortical columnar organization and reduced orientation selectivity in the visual cortex. J Neurophysiol 93:1317-1325.
40. Meister M, Wong ROL, Baylor DA, Shatz CJ (1991) Synchronous bursts of action potentials in ganglion cells of the developing mammalian retina. Science 252:939-943.
41. Meister M, Pine J, Baylor DA (1994) Multi-neuronal signals from the retina: acquisition and analysis. J Neurosci Methods 51:95-106.
42. Mitchell SJ, Silver RA (2003) Shunting inhibition modulates neuronal gain during synaptic excitation. Neuron 38:433-445.
43. Mody I (2001) Distinguishing between GABA(A) receptors responsible for tonic and phasic conductances. Neurochem Res 26:907-913.
44. Mody I (2005) Aspects of the homeostaic plasticity of GABAA receptor-mediated inhibition. J Physiol (Lond) 562:37-46.
45. Mody I, Pearce RA (2004) Diversity of inhibitory neurotransmission through GABA(A) receptors. Trends Neurosci 27:569-575.
46. Myhr KL, Lukasiewicz PD, Wong RO (2001) Mechanisms underlying developmental changes in the firing patterns of ON and OFF retinal ganglion cells during refinement of their central projections. J Neurosci 21:8664-8671.
47. Neher E (1992) Correction for liquid junction potentials in patch clamp experiments. Methods Enzymol 207:123-131.
48. O'Donovan MJ (1999) The origin of spontaneous activity in developing networks of the vertebrate nervous system. Curr Opin Neurobiol 9:94-104.
49. Owens DF, Kriegstein AR (2002) Is there more to GABA than synaptic inhibition? Nat Rev Neurosci 3:715-727.
50. Payne JA, Rivera C, Voipio J, Kaila K (2003) Cation-chloride cotransporters in neuronal communication, development and trauma. Trends Neurosci 26:199-206.
51. Represa A, Ben-Ari Y (2005) Trophic actions of GABA on neuronal development. Trends Neurosci 28:278-283.
52. Rivera C, Voipio J, Payne JA, Ruusuvuori E, Lahtinen H, Lamsa K, Pirvola U, Saarma M, Kaila K (1999) The K+/Cl- co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 397:251-255.
53. Semyanov A, Walker MC, Kullmann DM (2003) GABA uptake regulates cortical excitability via cell type-specific tonic inhibition. Nat Neurosci 6:484-490.
54. Semyanov A, Walker MC, Kullmann DM, Silver RA (2004) Tonically active GABA A receptors: modulating gain and maintaining the tone. Trends Neurosci 27:262-269.
55. Sernagor E, Young C, Eglen SJ (2003) Developmental modulation of retinal wave dynamics: shedding light on the GABA saga. J Neurosci 23:7621-7629.
56. Singer J, Mirotznik R, Feller M (2001) Potentiation of L-type calcium channels reveals nonsynaptic mechanisms that correlate spontaneous activity in the developing mammalian retina. J Neurosci 21:8514-8522.
57. Soda T, Nakashima R, Watanabe D, Nakajima K, Pastan I, Nakanishi S (2003) Segregation and coactivation of developing neocortical layer 1 neurons. J Neurosci 23:6272-6279.
58. Stella Jr SL, Bryson EJ, Cadetti L, Thoreson WB (2003) Endogenous adenosine reduces glutamatergic output from rods through activation of A2-like adenosine receptors. J Neurophysiol 90:165-174.
59. Stellwagen D, Shatz CJ, Feller MB (1999) Dynamics of retinal waves are controlled by cyclic AMP. Neuron 24:673-685.
60. Stromland K (2004) Visual impairment and ocular abnormalities in children with fetal alcohol syndrome. Addict Biol 9:153-157; discussion 159-160.
61. Syed MM, Lee S, He S, Zhou ZJ (2004a) Spontaneous waves in the ventricular zone of developing mammalian retina. J Neurophysiol 91:1999-2009.
62. Syed MM, Lee S, Zheng J, Zhou ZJ (2004b) Stage-dependent dynamics and modulation of spontaneous waves in the developing rabbit retina. J Physiol (Lond) 560:533-549.
63. Torborg CL, Feller MB (2005) Spontaneous patterned retinal activity and the refinement of retinal projections. Prog Neurobiol 76:213-235.
64. Torborg CL, Hansen KA, Feller MB (2005) High frequency, synchronized bursting drives eye-specific segregation of retinogeniculate projections. Nat Neurosci 8:72-78.
65. Tozuka Y, Fukuda S, Namba T, Seki T, Hisatsune T (2005) GABAergic excitation promotes neuronal differentiation in adult hippocampal progenitor cells. Neuron 47:803-815.
66. Wassle H, Koulen P, Brandstatter JH, Fletcher EL, Becker CM (1998) Glycine and GABA receptors in the mammalian retina. Vision Res 38:1411-1430.
67. Watanabe D, Inokawa H, Hashimoto K, Suzuki N, Kano M, Shigemoto R, Hirano T, Toyama K, Kaneko S, Yokoi M, Moriyoshi K, Suzuki M, Kobayashi K, Nagatsu T, Kreitman RJ, Pastan I, Nakanishi S (1998) Ablation of cerebellar Golgi cells disrupts synaptic integration involving GABA inhibition and NMDA receptor activation in motor coordination. Cell 95:17-27.
68. Weiner JL, Valenzuela CF (2006) Ethanol modulation of GABAergic transmission: the view from the slice. Pharmacol Ther 111:533-554.
69. Wetherington JP, Lambert NA (2002) Differential desensitization of responses mediated by presynaptic and postsynaptic A1 adenosine receptors. J Neurosci 22:1248-1255.
70. Whittington MA, Traub RD (2003) Interneuron diversity series: inhibitory interneurons and network oscillations in vitro. Trends Neurosci 26:676-682.
71. Wong R (1999) Retinal waves and visual system development. Annu Rev Neurosci 22:29-47.
72. Wong RO, Oakley DM (1996) Changing patterns of spontaneous bursting activity of on and off retinal ganglion cells during development. Neuron 16:1087-1095.
73. Wong RO, Meister M, Shatz CJ (1993) Transient period of correlated bursting activity during development of the mammalian retina. Neuron 11:923-938.
74. Yoshida K, Watanabe D, Ishikane H, Tachibana M, Pastan I, Nakanishi S (2001) A key role of starburst amacrine cells in originating retinal directional selectivity and optokinetic eye movement. Neuron 30:771-780.
75. Zhang LL, Pathak HR, Coulter DA, Freed MA, Vardi N (2006) Shift of intracellular chloride concentration in ganglion and amacrine cells of developing mouse retina. J Neurophysiol 95:2404-2416.
76. Zheng J, Lee S, Zhou ZJ (2006) A transient network of intrinsically bursting starburst cells underlies the generation of retinal waves. Nat Neurosci 9:363-371.
77. Zheng JJ, Lee S, Zhou ZJ (2004) A developmental switch in the excitability and function of the starburst network in the mammalian retina. Neuron 44:851-864.
78. Zhou Z (2001) The function of the cholinergic system in the developing mammalian retina. Prog Brain Res 131:599-613.
79. Zhou ZJ (1998) Direct participation of starburst amacrine cells in spontaneous rhythmic activities in the developing mammalian retina. J Neurosci 18:4155-4165.
80. Zucker CL, Ehinger B (1998) Gamma-aminobutyric acidA receptors on a bistratified amacrine cell type in the rabbit retina. J Comp Neurol 393:309-319.