GABAA receptor-mediated tonic depolarization in developing neural circuits

Molecular Neurobiology

Volumn 49, Issue 2, 2014, Pages 702-723

  Lu, Juu Chin ^a   Hsiao, Yu Tien ^b   Chiang, Chung Wei ^b   Wang, Chih Tien ^b  

^a CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

^b NATIONAL TAIWAN UNIVERSITY   (Taiwan)

Author keywords

Activity dependent gene expression; Neural circuit refinement; Patterned spontaneous activity; Shunting inhibition

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; CALCIUM ION;

AUDITORY SYSTEM; BIOCHEMICAL COMPOSITION; CELLULAR PARAMETERS; CEREBELLUM; DEPOLARIZATION; DEVELOPMENTAL STAGE; HIPPOCAMPUS; HUMAN; KNOWLEDGE DISCOVERY; MOLECULAR MECHANICS; NEUROMODULATION; NEUROTRANSMISSION; NONHUMAN; RETINA; REVIEW; SHUNTING INHIBITION; SPINAL CORD; ACTION POTENTIAL; ANIMAL; BRAIN; GROWTH, DEVELOPMENT AND AGING; NERVE CELL INHIBITION; NERVE CELL NETWORK; PHYSIOLOGY;

ACTION POTENTIALS; ANIMALS; BRAIN; HUMANS; NERVE NET; NEURAL INHIBITION; RECEPTORS, GABA-A;

EID: 84896542830     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-013-8548-x     Document Type: Review

References (261)

1. Erlander MG, Tillakaratne NJ, Feldblum S, Patel N, Tobin AJ (1991) Two genes encode distinct glutamate decarboxylases. Neuron 7(1):91-100
2. Roth FC, Draguhn A (2012) GABA metabolism and transport: effects on synaptic efficacy. Neural Plast 2012:805830
3. Gassmann M, Bettler B (2012) Regulation of neuronal GABA(B) receptor functions by subunit composition. Nat Rev Neurosci 13(6):380-394
4. Attwell D, Barbour B, Szatkowski M (1993) Nonvesicular release of neurotransmitter. Neuron 11(3):401-407 (Pubitemid 23287068)
5. Taylor J, Gordon-Weeks PR (1991) Calcium-independent gamma-aminobutyric acid release from growth cones: role of gamma-aminobutyric acid transport. J Neurochem 56(1):273-280 (Pubitemid 21901960)
6. Rudolph U, Mohler H (2004) Analysis of GABAA receptor function and dissection of the pharmacology of benzodiazepines and general anesthetics through mouse genetics. Annu Rev Pharmacol Toxicol 44:475-498 (Pubitemid 38263850)
7. Belelli D, Lambert JJ (2005) Neurosteroids: endogenous regulators of the GABA(A) receptor. Nat Rev Neurosci 6(7):565-575 (Pubitemid 40942823)
8. Follesa P, Biggio F, Talani G, Murru L, Serra M, Sanna E, Biggio G (2006) Neurosteroids, GABAA receptors, and ethanol dependence. Psychopharmacology (Berl) 186(3):267-280 (Pubitemid 43800829)
9. Simon J, Wakimoto H, Fujita N, Lalande M, Barnard EA (2004) Analysis of the set of GABA(A) receptor genes in the human genome. J Biol Chem 279(40):41422-41435 (Pubitemid 39313583)
10. Olsen RW, Sieghart W (2008) International Union of Pharmacology. LXX. Subtypes of gamma-aminobutyric acid(A) receptors: classification on the basis of subunit composition, pharmacology, and function. Update. Pharmacol Rev 60(3):243-260
11. Chen ZW, Olsen RW (2007) GABAA receptor associated proteins: a key factor regulating GABAA receptor function. J Neurochem 100(2):279-294
12. 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(5):331-343 (Pubitemid 351556042)
13. Koulen P, Sassoe-Pognetto M, Grunert U, Wassle H (1996) Selective clustering of GABA(A) and glycine receptors in the mammalian retina. J Neurosci 16(6):2127-2140
14. Semyanov A, Walker MC, Kullmann DM, Silver RA (2004) Tonically active GABA A receptors: modulating gain and maintaining the tone. Trends Neurosci 27(5):262-269 (Pubitemid 38529954)
15. Belelli D, Harrison NL, Maguire J, Macdonald RL, Walker MC, Cope DW (2009) Extrasynaptic GABAA receptors: form, pharmacology, and function. J Neurosci 29(41):12757-12763
16. Herd MB, Haythornthwaite AR, Rosahl TW, Wafford KA, Homanics GE, Lambert JJ, Belelli D (2008) The expression of GABAA beta subunit isoforms in synaptic and extrasynaptic receptor populations of mouse dentate gyrus granule cells. J Physiol 586(4):989-1004 (Pubitemid 351267341)
17. Saliba RS, Kretschmannova K, Moss SJ (2012) Activity-dependent phosphorylation of GABAA receptors regulates receptor insertion and tonic current. EMBO J 31(13):2937-2951
18. Farrant M, Nusser Z (2005) Variations on an inhibitory theme: phasic and tonic activation of GABA(A) receptors. Nat Rev Neurosci 6(3):215-229 (Pubitemid 40342416)
19. Rossi DJ, Hamann M (1998) Spillover-mediated transmission at inhibitory synapses promoted by high affinity alpha6 subunit GABA(A) receptors and glomerular geometry. Neuron 20(4):783-795 (Pubitemid 28199056)
20. Huss M, Ingenhorst G, Konig S, Gassel M, Drose S, Zeeck A, Altendorf K, Wieczorek H (2002) Concanamycin A, the specific inhibitor of V-ATPases, binds to the V(o) subunit c. J Biol Chem 277(43):40544-40548 (Pubitemid 35215633)
21. Tang ZQ, Dinh EH, Shi W, Lu Y (2011) Ambient GABA-activated tonic inhibition sharpens auditory coincidence detection via a depolarizing shunting mechanism. J Neurosci 31(16):6121-6131
22. Semyanov A, Walker MC, Kullmann DM (2003) GABA uptake regulates cortical excitability via cell type-specific tonic inhibition. Nat Neurosci 6(5):484-490 (Pubitemid 36514696)
23. 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(4):2690-2701 (Pubitemid 37266533)
24. Keros S, Hablitz JJ (2005) Subtype-specific GABA transporter antagonists synergistically modulate phasic and tonic GABAA conductances in rat neocortex. J Neurophysiol 94(3):2073-2085 (Pubitemid 41192878)
25. Ben-Ari Y (2002) Excitatory actions of gaba during development: the nature of the nurture. Nat Rev Neurosci 3(9):728-739
26. Hamann M, Rossi DJ, Attwell D (2002) Tonic and spillover inhibition of granule cells control information flow through cerebellar cortex. Neuron 33(4):625-633 (Pubitemid 34188437)
27. Mitchell SJ, Silver RA (2003) Shunting inhibition modulates neuronal gain during synaptic excitation. Neuron 38(3):433-445 (Pubitemid 36579145)
28. Chadderton P, Margrie TW, Hausser M (2004) Integration of quanta in cerebellar granule cells during sensory processing. Nature 428(6985):856-860 (Pubitemid 38529500)
29. Cope DW, Hughes SW, Crunelli V (2005) GABAA receptor-mediated tonic inhibition in thalamic neurons. J Neurosci 25(50):11553-11563 (Pubitemid 43098448)
30. Wolfart J, Debay D, Le Masson G, Destexhe A, Bal T (2005) Synaptic background activity controls spike transfer from thalamus to cortex. Nat Neurosci 8(12):1760-1767 (Pubitemid 41683205)
31. Park JB, Skalska S, Stern JE (2006) Characterization of a novel tonic gamma-aminobutyric acidA receptor-mediated inhibition in magnocellular neurosecretory neurons and its modulation by glia. Endocrinology 147(8):3746-3760 (Pubitemid 44079379)
32. Bright DP, Aller MI, Brickley SG (2007) Synaptic release generates a tonic GABA(A) receptor-mediated conductance that modulates burst precision in thalamic relay neurons. J Neurosci 27(10):2560-2569 (Pubitemid 46393585)
33. Wang CT, Blankenship AG, Anishchenko A, Elstrott J, Fikhman M, Nakanishi S, Feller MB (2007) GABAA receptor-mediated signaling alters the structure of spontaneous activity in the developing retina. J Neurosci 27(34):9130-9140 (Pubitemid 47312057)
34. Rothman JS, Cathala L, Steuber V, Silver RA (2009) Synaptic depression enables neuronal gain control. Nature 457(7232):1015-1018
35. 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 497(Pt 3):753-759
36. Wall MJ, Usowicz MM (1997) Development of action potential-dependent and independent spontaneous GABAA receptor-mediated currents in granule cells of postnatal rat cerebellum. Eur J Neurosci 9(3):533-548
37. Nusser Z, Sieghart W, Somogyi P (1998) Segregation of different GABAA receptors to synaptic and extrasynaptic membranes of cerebellar granule cells. J Neurosci 18(5):1693-1703 (Pubitemid 28103077)
38. Brickley SG, Revilla V, Cull-Candy SG, Wisden W, Farrant M (2001) Adaptive regulation of neuronal excitability by a voltage-independent potassium conductance. Nature 409(6816):88-92. doi:10.1038/35051086 (Pubitemid 32098630)
39. Bai D, Zhu G, Pennefather P, Jackson MF, MacDonald JF, Orser BA (2001) Distinct functional and pharmacological properties of tonic and quantal inhibitory postsynaptic currents mediated by gamma-aminobutyric acid(A) receptors in hippocampal neurons. Mol Pharmacol 59(4):814-824 (Pubitemid 32274010)
40. Nusser Z, Mody I (2002) Selective modulation of tonic and phasic inhibitions in dentate gyrus granule cells. J Neurophysiol 87(5):2624-2628 (Pubitemid 34670732)
41. Wei W, Zhang N, Peng Z, Houser CR, Mody I (2003) Perisynaptic localization of delta subunit-containing GABA(A) receptors and their activation by GABA spillover in the mouse dentate gyrus. J Neurosci 23(33):10650-10661 (Pubitemid 37485279)
42. Caraiscos VB, Newell JG, You-Ten KE, Elliott EM, Rosahl TW, Wafford KA, MacDonald JF, Orser BA (2004) Selective enhancement of tonic GABAergic inhibition in murine hippocampal neurons by low concentrations of the volatile anesthetic isoflurane. J Neurosci 24(39):8454-8458 (Pubitemid 39313767)
43. Scimemi A, Semyanov A, Sperk G, Kullmann DM, Walker MC (2005) Multiple and plastic receptors mediate tonic GABAA receptor currents in the hippocampus. J Neurosci 25(43):10016-10024 (Pubitemid 41528040)
44. Glykys J, Peng Z, Chandra D, Homanics GE, Houser CR, Mody I (2007) A new naturally occurring GABA(A) receptor subunit partnership with high sensitivity to ethanol. Nat Neurosci 10(1):40-48 (Pubitemid 46026526)
45. Drasbek KR, Jensen K (2006) THIP, a hypnotic and antinociceptive drug, enhances an extrasynaptic GABAA receptor-mediated conductance in mouse neocortex. Cereb Cortex 16(8):1134-1141 (Pubitemid 44025383)
46. Yamada J, Furukawa T, Ueno S, Yamamoto S, Fukuda A (2007) Molecular basis for the GABAA receptor-mediated tonic inhibition in rat somatosensory cortex. Cereb Cortex 17(8):1782-1787 (Pubitemid 47216495)
47. Krook-Magnuson EI, Li P, Paluszkiewicz SM, Huntsman MM (2008) Tonically active inhibition selectively controls feedforward circuits in mouse barrel cortex. J Neurophysiol 100(2):932-944
48. Belelli D, Peden DR, Rosahl TW, Wafford KA, Lambert JJ (2005) Extrasynaptic GABAA receptors of thalamocortical neurons: a molecular target for hypnotics. J Neurosci 25(50):11513-11520 (Pubitemid 43098444)
49. Jia F, Pignataro L, Schofield CM, Yue M, Harrison NL, Goldstein PA (2005) An extrasynaptic GABAA receptor mediates tonic inhibition in thalamic VB neurons. J Neurophysiol 94(6):4491-4501 (Pubitemid 41691802)
50. Takahashi A, Mashimo T, Uchida I (2006) GABAergic tonic inhibition of substantia gelatinosa neurons in mouse spinal cord. NeuroReport 17(12):1331-1335 (Pubitemid 44337077)
51. Wang L, Spary E, Deuchars J, Deuchars SA (2008) Tonic GABAergic inhibition of sympathetic preganglionic neurons: a novel substrate for sympathetic control. J Neurosci 28(47):12445-12452
52. Park JB, Skalska S, Son S, Stern JE (2007) Dual GABAA receptor-mediated inhibition in rat presympathetic paraventricular nucleus neurons. J Physiol 582(Pt 2):539-551 (Pubitemid 47040543)
53. Zhang SJ, Jackson MB (1993) GABA-activated chloride channels in secretory nerve endings. Science 259(5094):531-534 (Pubitemid 23058714)
54. Ade KK, Janssen MJ, Ortinski PI, Vicini S (2008) Differential tonic GABA conductances in striatal medium spiny neurons. J Neurosci 28(5):1185-1197 (Pubitemid 351186342)
55. Janssen MJ, Ade KK, Fu Z, Vicini S (2009) Dopamine modulation of GABA tonic conductance in striatal output neurons. J Neurosci 29(16):5116-5126
56. Janssen MJ, Yasuda RP, Vicini S (2011) GABA(A) Receptor beta3 subunit expression regulates tonic current in developing striatopallidal medium spiny neurons. Front Cell Neurosci 5:15
57. Pavlov I, Walker MC (2012) Tonic GABA(A) receptor-mediated signalling in temporal lobe epilepsy. Neuropharmacology
58. Curia G, Papouin T, Seguela P, Avoli M (2009) Downregulation of tonic GABAergic inhibition in amouse model of fragile X syndrome. Cereb Cortex 19(7):1515-1520
59. Olmos-Serrano JL, Paluszkiewicz SM, Martin BS, Kaufmann WE, Corbin JG, Huntsman MM (2010) Defective GABAergic neurotransmission and pharmacological rescue of neuronal hyperexcitability in the amygdala in a mouse model of fragile X syndrome. J Neurosci 30(29):9929-9938
60. Shen H, Gong QH, Aoki C, Yuan M, Ruderman Y, Dattilo M, Williams K, Smith SS (2007) Reversal of neurosteroid effects at alpha4beta2delta GABAA receptors triggers anxiety at puberty. Nat Neurosci 10(4):469-477 (Pubitemid 46494589)
61. Maguire J, Mody I (2007) Neurosteroid synthesis-mediated regulation of GABA(A) receptors: relevance to the ovarian cycle and stress. J Neurosci 27(9):2155-2162 (Pubitemid 46340948)
62. Laviolette SR, Gallegos RA, Henriksen SJ, van der Kooy D (2004) Opiate state controls bi-directional reward signaling via GABAA receptors in the ventral tegmental area. Nat Neurosci 7(2):160-169 (Pubitemid 38129792)
63. Vargas-Perez H, Ting AKR, Walton CH, Hansen DM, Razavi R, Clarke L, Bufalino MR, Allison DW, Steffensen SC, van der Kooy D (2009) Ventral tegmental area BDNF induces an opiate-dependent-like reward state in naive rats. Science 324(5935):1732-1734
64. Maguire JL, Stell BM, Rafizadeh M, Mody I (2005) Ovarian cycle-linked changes in GABA(A) receptors mediating tonic inhibition alter seizure susceptibility and anxiety. Nat Neurosci 8(6):797-804 (Pubitemid 43085847)
65. Maguire J, Mody I (2008) GABA(A)R plasticity during pregnancy: relevance to postpartum depression. Neuron 59(2):207-213 (Pubitemid 352033688)
66. - co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 397(6716):251-255
67. Payne JA, Rivera C, Voipio J, Kaila K (2003) Cation-chloride co-transporters in neuronal communication, development and trauma. Trends Neurosci 26(4):199-206 (Pubitemid 36412002)
68. Owens DF, Kriegstein AR (2002) Is there more to GABA than synaptic inhibition? Nat Rev Neurosci 3(9):715-727 (Pubitemid 135706677)
69. Akerman CJ, Cline HT (2007) Refining the roles of GABAergic signaling during neural circuit formation. Trends Neurosci 30(8):382-389 (Pubitemid 47088714)
70. Zhang LL, Fina ME, Vardi N (2006) Regulation of KCC2 and NKCC during development: membrane insertion and differences between cell types. J Comp Neurol 499(1):132-143 (Pubitemid 44423700)
71. Sernagor E, Young C, Eglen SJ (2003) Developmental modulation of retinal wave dynamics: shedding light on the GABA saga. J Neurosci 23(20):7621-7629 (Pubitemid 37034079)
72. Ganguly K, Schinder AF, Wong ST, Poo M (2001) GABA itself promotes the developmental switch of neuronal GABAergic responses from excitation to inhibition. Cell 105(4):521-532 (Pubitemid 32520857)
73. Tyzio R, Cossart R, Khalilov I, Minlebaev M, Hubner CA, Represa A, Ben-Ari Y, Khazipov R (2006) Maternal oxytocin triggers a transient inhibitory switch in GABA signaling in the fetal brain during delivery. Science 314(5806):1788-1792 (Pubitemid 44969093)
74. van den Pol AN, Obrietan K, Chen G (1996) Excitatory actions of GABA after neuronal trauma. J Neurosci 16(13):4283-4292 (Pubitemid 26192423)
75. Nabekura J, Ueno T, Okabe A, Furuta A, Iwaki T, Shimizu-Okabe C, Fukuda A, Akaike N (2002) Reduction of KCC2 expression and GABAA receptor-mediated excitation after in vivo axonal injury. J Neurosci 22(11):4412-4417 (Pubitemid 37465658)
76. Coull JA, Boudreau D, Bachand K, Prescott SA, Nault F, Sik A, De Koninck P, De Koninck Y (2003) Trans-synaptic shift in anion gradient in spinal lamina I neurons as a mechanism of neuropathic pain. Nature 424(6951):938-942 (Pubitemid 37051684)
77. Vale C, Schoorlemmer J, Sanes DH (2003) Deafness disrupts chloride transporter function and inhibitory synaptic transmission. J Neurosci 23(20):7516-7524 (Pubitemid 37034068)
78. Topolnik L, Steriade M, Timofeev I (2003) Hyperexcitability of intact neurons underlies acute development of trauma-related electrographic seizures in cats in vivo. Eur J Neurosci 18(3):486-496 (Pubitemid 37041100)
79. Huberfeld G, Wittner L, Clemenceau S, Baulac M, Kaila K, Miles R, Rivera C (2007) Perturbed chloride homeostasis and GABAergic signaling in human temporal lobe epilepsy. J Neurosci 27(37):9866-9873 (Pubitemid 47404011)
80. Represa A, Ben-Ari Y (2005) Trophic actions of GABA on neuronal development. Trends Neurosci 28(6):278-283 (Pubitemid 40775771)
81. Ben-Ari Y, Gaiarsa JL, Tyzio R, Khazipov R (2007) GABA: a pioneer transmitter that excites immature neurons and generates primitive oscillations. Physiol Rev 87(4):1215-1284 (Pubitemid 350041471)
82. Sernagor E, Chabrol F, Bony G, Cancedda L (2010) GABAergic control of neurite outgrowth and remodeling during development and adult neurogenesis: general rules and differences in diverse systems. Front Cell Neurosci 4:11
83. Penn AA, Shatz CJ (1999) Brain waves and brain wiring: the role of endogenous and sensory-driven neural activity in development. Pediatr Res 45(4 Pt 1):447-458 (Pubitemid 29162722)
84. Xu HP, Furman M, Mineur YS, Chen H, King SL, Zenisek D, Zhou ZJ, Butts DA, Tian N, Picciotto MR, Crair MC (2011) An instructive role for patterned spontaneous retinal activity in mouse visual map development. Neuron 70(6):1115-1127
85. Zhang J, Ackman JB, Dhande OS, Crair MC (2011) Visualization and manipulation of neural activity in the developing vertebrate nervous system. Front Mol Neurosci 4:43
86. Zhang J, Ackman JB, Xu HP, Crair MC (2011) Visual map development depends on the temporal pattern of binocular activity in mice. Nat Neurosci 15:298-307
87. Lewis DA, Levitt P (2002) Schizophrenia as a disorder of neurodevelopment. Annu Rev Neurosci 25:409-432 (Pubitemid 34748023)
88. Patterson PH (2007) Neuroscience. Maternal effects on schizophrenia risk. Science 318(5850):576-577
89. Blankenship AG, Feller MB (2010) Mechanisms underlying spontaneous patterned activity in developing neural circuits. Nat Rev Neurosci 11(1):18-29
90. Ben-Ari Y (2001) Developing networks play a similar melody. Trends Neurosci 24(6):353-360
91. Bosma MM (2010) Timing and mechanism of a window of spontaneous activity in embryonic mouse hindbrain development. Ann N YAcad Sci 1198:182-191
92. Wong RO (1999) Retinal waves and visual system development. Annu Rev Neurosci 22:29-47
93. Huberman AD, Feller MB, Chapman B (2008) Mechanisms underlying development of visual maps and receptive fields. Annu Rev Neurosci 31:479-509
94. Gonzalez-Islas C, Chub N, Garcia-Bereguiain MA, Wenner P (2010) GABAergic synaptic scaling in embryonic motoneurons is mediated by a shift in the chloride reversal potential. J Neurosci 30(39):13016-13020
95. Grasshoff C, Netzhammer N, Schweizer J, Antkowiak B, Hentschke H (2008) Depression of spinal network activity by thiopental: shift from phasic to tonic GABA(A) receptor-mediated inhibition. Neuropharmacology 55(5):793-802
96. 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 581(Pt 2):515-528 (Pubitemid 46831753)
97. 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(4):1318-1335 (Pubitemid 24121832)
98. Neher E (1992) Correction for liquid junction potentials in patch clamp experiments. Methods Enzymol 207:123-131
99. Mooney R, PennAA, Gallego R, Shatz CJ (1996) Thalamic relay of spontaneous retinal activity prior to vision. Neuron 17:979-990
100. Weliky M, Katz LC (1999) Correlational structure of spontaneous neuronal activity in the developing lateral geniculate nucleus in vivo. Science 285(5427):599-604
101. Hanganu IL, Ben-Ari Y, Khazipov R (2006) Retinal waves trigger spindle bursts in the neonatal rat visual cortex. J Neurosci 26(25):6728-6736 (Pubitemid 44315234)
102. Ackman JB, Burbridge TJ, Crair MC (2012) Retinal waves coordinate patterned activity throughout the developing visual system. Nature 490(7419):219-225
103. Ford KJ, Feller MB (2011) Assembly and disassembly of a retinal cholinergic network. Vis Neurosci 29(1):61-71
104. Syed MM, Lee S, Zheng J, Zhou ZJ (2004) Stage-dependent dynamics and modulation of spontaneous waves in the developing rabbit retina. J Physiol 560(Pt 2):533-549 (Pubitemid 39440113)
105. Feller M, Wellis D, Stellawagen D, Werblin F, Shatz C (1996) Requirement for cholinergic synaptic transmission in the propagation of spontaneous retinal waves. Science 272:1181-1197
106. Fischer KF, Lukasiewicz PD, Wong RO (1998) Age-dependent and cell class-specific modulation of retinal ganglion cell bursting activity by GABA. J Neurosci 18(10):3767-3778 (Pubitemid 28225684)
107. Stellwagen D, Shatz C, Feller M (1999) Dynamics of retinal waves are controlled by cyclic AMP. Neuron 24:673-685
108. 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(2):518-529 (Pubitemid 36139551)
109. 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(4):2404-2416
110. Firth SI, Wang CT, Feller MB (2005) Retinal waves: mechanisms and function in visual system development. Cell Calcium 37(5):425-432 (Pubitemid 40458439)
111. Zhou ZJ (1998) Direct participation of starburst amacrine cells in spontaneous rhythmic activities in the developing mammalian retina. J Neurosci 18(11):4155-4165
112. 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(5):851-864 (Pubitemid 39575637)
113. 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(2):539-548 (Pubitemid 46147919)
114. 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(1):71-73 (Pubitemid 23349397)
115. Mody I, Pearce RA (2004) Diversity of inhibitory neurotransmission through GABA(A) receptors. Trends Neurosci 27(9):569-575 (Pubitemid 39149827)
116. Greferath U, Grunert U, Fritschy JM, Stephenson A, Mohler H, Wassle H (1995) GABAA receptor subunits have differential distributions in the rat retina: in situ hybridization and immunohistochemistry. J Comp Neurol 353(4):553-571
117. Khan ZU, Gutierrez A, Mehta AK, Miralles CP, De Blas AL (1996) The [alpha]4 subunit of the GABAA receptors from rat brain and retina. Neuropharmacology 35(9-10):1315
118. Chiang CW, Chen YC, Lu JC, Hsiao YT, Chang CW, Huang PC, Chang YT, Chang PY, Wang CT (2012) Synaptotagmin I regulates patterned spontaneous activity in the developing rat retina via calcium binding to the C2AB domains. PLoS One 7(10):e47465
119. Zheng J, Lee S, Zhou ZJ (2006) A transient network of intrinsically bursting starburst cells underlies the generation of retinal waves.Nat Neurosci 9(3):363-371 (Pubitemid 43290966)
120. Ford KJ, Felix AL, Feller MB (2012) Cellular mechanisms underlying spatiotemporal features of cholinergic retinal waves. J Neurosci 32(3):850-863
121. Yamasaki EN, Barbosa VD, De Mello FG, Hokoc JN (1999) GABAergic system in the developing mammalian retina: dual sources of GABA at early stages of postnatal development. Int J Dev Neurosci 17(3):201-213 (Pubitemid 29287272)
122. Macdonald RL, Olsen RW (1994) GABAA receptor channels. Annu Rev Neurosci 17:569-602
123. Veruki ML, Yeh HH (1992) Vasoactive intestinal polypeptide modulates GABAA receptor function in bipolar cells and ganglion cells of the rat retina. J Neurophysiol 67(4):791-797
124. Feigenspan A, Bormann J (1994) Facilitation of GABAergic signaling in the retina by receptors stimulating adenylate cyclase. Proc Natl Acad Sci U S A 91(23):10893-10897 (Pubitemid 24349591)
125. Hoon M, Bauer G, Fritschy JM, Moser T, Falkenburger BH, Varoqueaux F (2009) Neuroligin 2 controls the maturation of GABAergic synapses and information processing in the retina. J Neurosci 29(25):8039-8050
126. Hoffpauir B, McMains E, Gleason E (2006) Nitric oxide transiently converts synaptic inhibition to excitation in retinal amacrine cells. J Neurophysiol 95(5):2866-2877
127. Staley KJ, Mody I (1992) Shunting of excitatory input to dentate gyrus granule cells by a depolarizing GABAA receptor-mediated postsynaptic conductance. J Neurophysiol 68(1):197-212
128. Ziskind-Conhaim L (1998) Physiological functions of GABA-induced depolarizations in the developing rat spinal cord. Perspect Dev Neurobiol 5(2-3):279-287
129. Zhang SJ, Jackson MB (1995) GABAA receptor activation and the excitability of nerve terminals in the rat posterior pituitary. J Physiol 483(Pt 3):583-595
130. Hensch TK, Fagiolini M (2005) Excitatory-inhibitory balance and critical period plasticity in developing visual cortex. Prog Brain Res 147:115-124
131. Wong RO, Oakley DM (1996) Changing patterns of spontaneous bursting activity of on and off retinal ganglion cells during development. Neuron 16(6):1087-1095 (Pubitemid 26227230)
132. 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(21):8664-8671 (Pubitemid 33051464)
133. Gao XB, Chen G, van den Pol AN (1998) GABA-dependent firing of glutamate-evoked action potentials at AMPA/kainate receptors in developing hypothalamic neurons. J Neurophysiol 79(2):716-726 (Pubitemid 28095891)
134. Lu T, Trussell LO (2001) Mixed excitatory and inhibitory GABA-mediated transmission in chick cochlear nucleus. J Physiol 535(Pt 1):125-131 (Pubitemid 32782730)
135. Calaza KC, Gardino PF, de Mello FG (2006) Transporter mediated GABA release in the retina: role of excitatory amino acids and dopamine. Neurochem Int 49(8):769-777 (Pubitemid 44648495)
136. Butts DA, Kanold PO, Shatz CJ (2007) A burst-based "Hebbian" learning rule at retinogeniculate synapses links retinal waves to activity-dependent refinement. PLoS Biol 5(3):e61
137. Chen C, Regehr WG (2000) Developmental remodeling of the retinogeniculate synapse. Neuron 28(3):955-966 (Pubitemid 32038084)
138. Mooney R, Madison DV, Shatz CJ (1993) Enhancement of transmission at the developing retinogeniculate synapse. Neuron 10(5):815-825 (Pubitemid 23152038)
139. Stellwagen D, Shatz CJ (2002) An instructive role for retinal waves in the development of retinogeniculate connectivity. Neuron 33:357-367 (Pubitemid 34158840)
140. Dunn TA, Wang CT, Colicos MA, Zaccolo M, DiPilato LM, Zhang J, Tsien RY, Feller MB (2006) Imaging of cAMP levels and protein kinase A activity reveals that retinal waves drive oscillations in second-messenger cascades. J Neurosci 26(49):12807-12815 (Pubitemid 44904576)
141. Dunn TA, Feller MB (2008) Imaging second messenger dynamics in developing neural circuits. Dev Neurobiol 68(6):835-844 (Pubitemid 351620775)
142. Pham TA, Rubenstein JL, Silva AJ, Storm DR, Stryker MP (2001) The CRE/CREB pathway is transiently expressed in thalamic circuit development and contributes to refinement of retinogeniculate axons. Neuron 31(3):409-420 (Pubitemid 32778560)
143. Shatz CJ, Stryker MP (1988) Prenatal tetrodotoxin infusion blocks segregation of retinogeniculate afferents. Science 242:87-89
144. Datwani A, McConnell MJ, Kanold PO, Micheva KD, Busse B, Shamloo M, Smith SJ, Shatz CJ (2009) Classical MHCI molecules regulate retinogeniculate refinement and limit ocular dominance plasticity. Neuron 64(4):463-470
145. Syken J, Grandpre T, Kanold PO, Shatz CJ (2006) PirB restricts ocular-dominance plasticity in visual cortex. Science 313(5794):1795-1800 (Pubitemid 44454157)
146. 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 (Pubitemid 33051450)
147. Torborg C, Wang CT, Muir-Robinson G, Feller MB (2004) L-type calcium channel agonist induces correlated depolarizations in mice lacking the beta2 subunit nAChRs. Vision Res 44(28):3347-3355 (Pubitemid 39469304)
148. Yuste R, Katz LC (1991) Control of postsynaptic Ca2+ influx in developing neocortex by excitatory and inhibitory neurotransmitters. Neuron 6(3):333-344
149. Lin MH, Takahashi MP, Takahashi Y, Tsumoto T (1994) Intracellular calcium increase induced by GABA in visual cortex of fetal and neonatal rats and its disappearance with development. Neurosci Res 20(1):85-94 (Pubitemid 24262421)
150. Leinekugel X, Tseeb V, Ben-Ari Y, Bregestovski P (1995) Synaptic GABAA activation induces Ca2+ rise in pyramidal cells and interneurons from rat neonatal hippocampal slices. J Physiol 487(Pt 2):319-329
151. Owens DF, Boyce LH, Davis MB, Kriegstein AR (1996) Excitatory GABA responses in embryonic and neonatal cortical slices demonstrated by gramicidin perforated-patch recordings and calcium imaging. J Neurosci 16(20):6414-6423 (Pubitemid 26337365)
152. Wei W, Hamby AM, Zhou K, Feller MB (2011) Development of asymmetric inhibition underlying direction selectivity in the retina. Nature 469(7330):402-406
153. Lippe WR (1994) Rhythmic spontaneous activity in the developing avian auditory system. J Neurosci 14(3 Pt 2):1486-1495
154. Jones TA, Jones SM, Paggett KC (2001) Primordial rhythmic bursting in embryonic cochlear ganglion cells. J Neurosci 21(20):8129-8135 (Pubitemid 32952769)
155. Tritsch NX, Yi E, Gale JE, Glowatzki E, Bergles DE (2007) The origin of spontaneous activity in the developing auditory system. Nature 450(7166):50-55 (Pubitemid 350070568)
156. Jones TA, Leake PA, Snyder RL, Stakhovskaya O, Bonham B (2007) Spontaneous discharge patterns in cochlear spiral ganglion cells before the onset of hearing in cats. J Neurophysiol 98(4):1898-1908 (Pubitemid 47584380)
157. Gummer AW, Mark RF (1994) Patterned neural activity in brain stem auditory areas of a prehearing mammal, the tammar wallaby (Macropus eugenii). NeuroReport 5(6):685-688 (Pubitemid 24110355)
158. Tritsch NX, Rodriguez-Contreras A, Crins TT, Wang HC, Borst JG, Bergles DE (2010) Calcium action potentials in hair cells pattern auditory neuron activity before hearing onset. Nat Neurosci 13(9):1050-1052
159. Tang ZQ, Gao H, Lu Y (2009) Control of a depolarizing GABAergic input in an auditory coincidence detection circuit. J Neurophysiol 102(3):1672-1683
160. Gabriele ML, Brunso-Bechtold JK, Henkel CK (2000) Plasticity in the development of afferent patterns in the inferior colliculus of the rat after unilateral cochlear ablation. J Neurosci 20(18):6939-6949
161. Leao RN, Sun H, Svahn K, Berntson A, Youssoufian M, Paolini AG, Fyffe RE, Walmsley B (2006) Topographic organization in the auditory brainstem of juvenile mice is disrupted in congenital deafness. J Physiol 571(Pt 3):563-578 (Pubitemid 43329547)
162. Leake PA, Hradek GT, Chair L, Snyder RL (2006) Neonatal deafness results in degraded topographic specificity of auditory nerve projections to the cochlear nucleus in cats. J Comp Neurol 497(1):13-31 (Pubitemid 43844565)
163. Kandler K (2004) Activity-dependent organization of inhibitory circuits: lessons from the auditory system. Curr Opin Neurobiol 14(1):96-104
164. O'Donovan MJ, Landmesser L (1987) The development of hindlimb motor activity studied in the isolated spinal cord of the chick embryo. J Neurosci 7(10):3256-3264
165. O'Donovan MJ, Wenner P, Chub N, Tabak J, Rinzel J (1998) Mechanisms of spontaneous activity in the developing spinal cord and their relevance to locomotion. Ann N YAcad Sci 860:130-141 (Pubitemid 29045965)
166. Nishimaru H, Iizuka M, Ozaki S, Kudo N (1996) Spontaneous motoneuronal activity mediated by glycine and GABA in the spinal cord of rat fetuses in vitro. J Physiol 497(Pt 1):131-143 (Pubitemid 26397678)
167. Ren J, Greer JJ (2003) Ontogeny of rhythmic motor patterns generated in the embryonic rat spinal cord. J Neurophysiol 89(3):1187-1195 (Pubitemid 36323966)
168. Hanson MG, Landmesser LT (2003) Characterization of the circuits that generate spontaneous episodes of activity in the early embryonic mouse spinal cord. J Neurosci 23(2):587-600 (Pubitemid 36139558)
169. Gonzalez-Islas C, Wenner P (2006) Spontaneous network activity in the embryonic spinal cord regulates AMPAergic and GABAergic synaptic strength. Neuron 49(4):563-575 (Pubitemid 43221891)
170. Hanson MG, Landmesser LT (2004) Normal patterns of spontaneous activity are required for correct motor axon guidance and the expression of specific guidance molecules. Neuron 43(5):687-701 (Pubitemid 39179728)
171. Hanson MG, Milner LD, Landmesser LT (2008) Spontaneous rhythmic activity in early chick spinal cord influences distinctmotor axon pathfinding decisions. Brain Res Rev 57(1):77-85 (Pubitemid 350213091)
172. Hanson MG, Landmesser LT (2006) Increasing the frequency of spontaneous rhythmic activity disrupts pool-specific axon fasciculation and pathfinding of embryonic spinalmotoneurons. J Neurosci 26(49):12769-12780 (Pubitemid 44904572)
173. Mochida H, Sato K, Arai Y, Sasaki S, Kamino K, Momose-Sato Y (2001) Optical imaging of spreading depolarization waves triggered by spinal nerve stimulation in the chick embryo: possible mechanisms for large-scale coactivation of the central nervous system. Eur J Neurosci 14(5):809-820
174. Momose-Sato Y, Sato K, Kinoshita M (2007) Spontaneous depolarization waves of multiple origins in the embryonic rat CNS. Eur J Neurosci 25(4):929-944
175. Xu H, Whelan PJ, Wenner P (2005) Development of an inhibitory interneuronal circuit in the embryonic spinal cord. J Neurophysiol 93(5):2922-2933 (Pubitemid 40570869)
176. Branchereau P, Chapron J, Meyrand P (2002) Descending 5-hydroxytryptamine raphe inputs repress the expression of serotonergic neurons and slow the maturation of inhibitory systems in mouse embryonic spinal cord. J Neurosci 22(7):2598-2606 (Pubitemid 37465809)
177. Wu WL, Ziskind-Conhaim L, Sweet MA (1992) Early development of glycine- and GABA-mediated synapses in rat spinal cord. J Neurosci 12(10):3935-3945
178. Sibilla S, Ballerini L (2009) GABAergic and glycinergic interneuron expression during spinal cord development: dynamic interplay between inhibition and excitation in the control of ventral network outputs. Prog Neurobiol 89(1):46-60
179. Chub N, Mentis GZ, O'Donovan MJ (2006) Chloride-sensitive MEQ fluorescence in chick embryo motoneurons following manipulations of chloride and during spontaneous network activity. J Neurophysiol 95(1):323-330 (Pubitemid 44698938)
180. Gonzalez-Islas C, Chub N, Wenner P (2009) NKCC1 and AE3 appear to accumulate chloride in embryonic motoneurons. J Neurophysiol 101(2):507-518
181. Wilhelm JC, Wenner P (2008) GABAA transmission is a critical step in the process of triggering homeostatic increases in quantal amplitude. Proc Natl Acad Sci U S A 105(32):11412-11417
182. Yoon YJ, Gokin AP, Martin-Caraballo M (2010) Pharmacological manipulation of GABA-driven activity in ovo disrupts the development of dendritic morphology but not the maturation of spinal cord network activity. Neural Dev 5:11
183. Persohn E, Malherbe P, Richards JG (1991) In situ hybridization histochemistry reveals a diversity of GABAA receptor subunit mRNAs in neurons of the rat spinal cord and dorsal root ganglia. Neuroscience 42(2):497-507
184. Wisden W, Gundlach AL, Barnard EA, Seeburg PH, Hunt SP (1991) Distribution of GABAA receptor subunit mRNAs in rat lumbar spinal cord. Brain Res Mol Brain Res 10(2):179-183
185. Bohlhalter S, Weinmann O, Mohler H, Fritschy JM (1996) Laminar compartmentalization of GABAA-receptor subtypes in the spinal cord: an immunohistochemical study. J Neurosci 16(1):283-297
186. Castro A, Aguilar J, Gonzalez-Ramirez R, Loeza-Alcocer E, Canto-Bustos M, Felix R, Delgado-Lezama R(2011) Tonic inhibition in spinal ventral horn interneurons mediated by alpha5 subunit-containing GABA(A) receptors. Biochem Biophys Res Commun 412(1):26-31
187. Levi S, Chesnoy-Marchais D, Sieghart W, Triller A (1999) Synaptic control of glycine and GABA(A) receptors and gephyrin expression in cultured motoneurons. J Neurosci 19(17):7434-7449 (Pubitemid 29404600)
188. Grasshoff C, Jurd R, Rudolph U, Antkowiak B (2007) Modulation of presynaptic beta3-containing GABAA receptors limits the immobilizing actions of GABAergic anesthetics. Mol Pharmacol 72(3):780-787 (Pubitemid 47347313)
189. Keller AF, Breton JD, Schlichter R, Poisbeau P (2004) Production of 5alpha-reduced neurosteroids is developmentally regulated and shapes GABA(A) miniature IPSCs in lamina II of the spinal cord. J Neurosci 24(4):907-915 (Pubitemid 38146601)
190. Mitchell EA, Gentet LJ, Dempster J, Belelli D (2007) GABAA and glycine receptor-mediated transmission in rat lamina II neurones: relevance to the analgesic actions of neuroactive steroids. J Physiol 583(Pt 3):1021-1040 (Pubitemid 47423714)
191. Poisbeau P, Patte-Mensah C, Keller AF, Barrot M, Breton JD, Luis-Delgado OE, Freund-Mercier MJ, Mensah-Nyagan AG, Schlichter R (2005) Inflammatory pain upregulates spinal inhibition via endogenous neurosteroid production. J Neurosci 25(50):11768-11776 (Pubitemid 43098469)
192. Inquimbert P, Rodeau JL, Schlichter R (2008) Regional differences in the decay kinetics of GABA(A) receptor-mediated miniature IPSCs in the dorsal horn of the rat spinal cord are determined by mitochondrial transport of cholesterol. J Neurosci 28(13):3427-3437 (Pubitemid 351469311)
193. Ballion B, Branchereau P, Chapron J, Viala D (2002) Ontogeny of descending serotonergic innervation and evidence for intraspinal 5-HT neurons in the mouse spinal cord. Brain Res Dev Brain Res 137(1):81-88 (Pubitemid 34786639)
194. Rajaofetra N, Sandillon F, Geffard M, Privat A (1989) Pre- and post-natal ontogeny of serotonergic projections to the rat spinal cord. J Neurosci Res 22(3):305-321 (Pubitemid 19112427)
195. Czarnecki A, Magloire V, Streit J (2009) Modulation of intrinsic spiking in spinal cord neurons. J Neurophysiol 102(4):2441-2452
196. Allain AE, Meyrand P, Branchereau P (2005) Ontogenic changes of the spinal GABAergic cell population are controlled by the serotonin (5-HT) system: implication of 5-HT1 receptor family. J Neurosci 25(38):8714-8724 (Pubitemid 41362050)
197. Bos R, Sadlaoud K, Boulenguez P, Buttigieg D, Liabeuf S, Brocard C, Haase G, Bras H, Vinay L (2012) Activation of 5-HT2A receptors upregulates the function of the neuronal K-Cl cotransporter KCC2. Proc Natl Acad Sci U S A 110(1):348-353
198. Cherubini E, Gaiarsa JL, Ben-Ari Y (1991) GABA: an excitatory transmitter in early postnatal life. Trends Neurosci 14(12):515-519
199. Ghosh A, Greenberg ME (1995) Calcium signaling in neurons: molecular mechanisms and cellular consequences. Science 268(5208):239-247
200. Spitzer NC (1994) Spontaneous Ca2+ spikes and waves in embryonic neurons: signaling systems for differentiation. Trends Neurosci 17(3):115-118
201. Gu X, Olson EC, Spitzer NC (1994) Spontaneous neuronal calcium spikes and waves during early differentiation. J Neurosci 14(11 Pt 1):6325-6335 (Pubitemid 24333056)
202. Watt SD, Gu X, Smith RD, Spitzer NC (2000) Specific frequencies of spontaneous Ca2+ transients upregulate GAD 67 transcripts in embryonic spinal neurons. Mol Cell Neurosci 16(4):376-387
203. Wang S, Polo-Parada L, Landmesser LT (2009) Characterization of rhythmic Ca2+ transients in early embryonic chick motoneurons: Ca2+ sources and effects of altered activation of transmitter receptors. J Neurosci 29(48):15232-15244
204. Leinekugel X, Khalilov I, Ben-Ari Y, Khazipov R (1998) Giant depolarizing potentials: the septal pole of the hippocampus paces the activity of the developing intact septohippocampal complex in vitro. J Neurosci 18(16):6349-6357 (Pubitemid 28373240)
205. 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(2):243-255 (Pubitemid 27111107)
206. - cotransport underlies plasticity of GABA(A) signaling in neonatal neurons. J Neurosci 28(6):1301-1312
207. Pfeffer CK, Stein V, Keating DJ, Maier H, Rinke I, Rudhard Y, Hentschke M, Rune GM, Jentsch TJ, Hubner CA (2009) NKCC1-dependent GABAergic excitation drives synaptic network maturation during early hippocampal development. J Neurosci 29(11):3419-3430
208. Valeeva G, Abdullin A, Tyzio R, Skorinkin A, Nikolski E, Ben-Ari Y, Khazipov R (2010) Temporal coding at the immature depolarizing GABAergic synapse. Front Cell Neurosci 4. doi:10.3389/fncel.2010.00017
209. Jagasia R, Steib K, Englberger E, Herold S, Faus-Kessler T, Saxe M, Gage FH, Song H, Lie DC (2009) GABA-cAMP response element-binding protein signaling regulatesmaturation and survival of newly generated neurons in the adult hippocampus. J Neurosci 29(25):7966-7977
210. 2+- and SNARE-independent release of GABA and glutamate prior to synapse formation. Neuron 36(6):1051-1061
211. Banke TG, McBain CJ (2006) GABAergic input onto CA3 hippocampal interneurons remains shunting throughout development. J Neurosci 26(45):11720-11725
212. Sipila ST, Huttu K, Soltesz I, Voipio J, Kaila K (2005) Depolarizing GABA acts on intrinsically bursting pyramidal neurons to drive giant depolarizing potentials in the immature hippocampus. J Neurosci 25(22):5280-5289 (Pubitemid 40770906)
213. Saliba RS, Michels G, Jacob TC, Pangalos MN, Moss SJ (2007) Activity-dependent ubiquitination of GABA(A) receptors regulates their accumulation at synaptic sites. J Neurosci 27(48):13341-13351 (Pubitemid 350220487)
214. Marchionni I, Kasap Z, Mozrzymas JW, Sieghart W, Cherubini E, Zacchi P (2009) New insights on the role of gephyrin in regulating both phasic and tonic GABAergic inhibition in rat hippocampal neurons in culture. Neuroscience 164(2):552-562
215. Sipila S, Huttu K, Voipio J, Kaila K (2004) GABA uptake via GABA transporter-1 modulates GABAergic transmission in the immature hippocampus. J Neurosci 24(26):5877-5880 (Pubitemid 38859384)
216. Khirug S, Huttu K, Ludwig A, Smirnov S, Voipio J, Rivera C, Kaila K, Khiroug L (2005) Distinct properties of functional KCC2 expression in immature mouse hippocampal neurons in culture and in acute slices. Eur J Neurosci 21(4):899-904 (Pubitemid 40461043)
217. - in and out of cells: implications for control of cell volume and neuronal excitability. Proc Natl Acad Sci U S A 102(46):16783-16788
218. Kahle KT, Rinehart J, Lifton RP (2010) Phosphoregulation of the Na-K-2Cl and K-Cl cotransporters by the WNK kinases. Biochim Biophys Acta 1802(12):1150-1158
219. He S, Ma J, Liu N, Yu X (2010) Early enriched environment promotes neonatal GABAergic neurotransmission and accelerates synapse maturation. J Neurosci 30(23):7910-7916
220. Chancey JH, Adlaf EW, Sapp MC, Pugh PC, Wadiche JI, Overstreet-Wadiche LS (2013) GABA depolarization is required for experience-dependent synapse unsilencing in adult-born neurons. J Neurosci 33(15):6614-6622
221. Bolea S, Avignone E, Berretta N, Sanchez-Andres JV, Cherubini E (1999) Glutamate controls the induction of GABA-mediated giant depolarizing potentials through AMPA receptors in neonatal rat hippocampal slices. J Neurophysiol 81(5):2095-2102 (Pubitemid 29262544)
222. de la Prida LM, Huberfeld G, Cohen I, Miles R (2006) Threshold behavior in the initiation of hippocampal population bursts. Neuron 49(1):131-142 (Pubitemid 43017191)
223. Watt AJ, Cuntz H, Mori M, Nusser Z, Sjostrom PJ, Hausser M (2009) Traveling waves in developing cerebellar cortex mediated by asymmetrical Purkinje cell connectivity. Nat Neurosci 12(4):463-473
224. Altman J (1972) Postnatal development of the cerebellar cortex in the rat. II. Phases in the maturation of Purkinje cells and of the molecular layer. J Comp Neurol 145(4):399-463
225. Hashimoto K, Kano M (2005) Postnatal development and synapse elimination of climbing fiber to Purkinje cell projection in the cerebellum. Neurosci Res 53(3):221-228 (Pubitemid 41463775)
226. Hashimoto K, Ichikawa R, Kitamura K, Watanabe M, Kano M (2009) Translocation of a "winner" climbing fiber to the Purkinje cell dendrite and subsequent elimination of "losers" from the soma in developing cerebellum. Neuron 63(1):106-118
227. Kano M, Hashimoto K (2009) Synapse elimination in the central nervous system. Curr Opin Neurobiol 19(2):154-161
228. 2+ channel in Purkinje cell mediates synaptic competition and elimination in developing cerebellum. Proc Natl Acad Sci U S A 108(24):9987-9992
229. Altman J (1972) Postnatal development of the cerebellar cortex in the rat. 3. Maturation of the components of the granular layer. J Comp Neurol 145(4):465-513
230. Carta M, Murru L, Barabino E, Talani G, Sanna E, Biggio G (2008) Isoniazid-induced reduction in GABAergic neurotransmission alters the function of the cerebellar cortical circuit. Neuroscience 154(2):710-719
231. Mameli M, Botta P, Zamudio PA, Zucca S, Valenzuela CF (2008) Ethanol decreases Purkinje neuron excitability by increasing GABA release in rat cerebellar slices. J Pharmacol Exp Ther 327(3):910-917
232. Tsutsui K (2008) Neurosteroids in the Purkinje cell: biosynthesis, mode of action and functional significance. Mol Neurobiol 37(2-3):116-125
233. Sasahara K, Shikimi H, Haraguchi S, Sakamoto H, Honda S, Harada N, Tsutsui K (2007) Mode of action and functional significance of estrogen-inducing dendritic growth, spinogenesis, and synaptogenesis in the developing Purkinje cell. J Neurosci 27(28):7408-7417 (Pubitemid 47071728)
234. Haraguchi S, Sasahara K, Shikimi H, Honda S, Harada N, Tsutsui K (2011) Estradiol promotes purkinje dendritic growth, spinogenesis, and synaptogenesis during neonatal life by inducing the expression of BDNF. Cerebellum 11(2):416-417
235. Griffin LD, Gong W, Verot L, Mellon SH (2004) Niemann-Pick type C disease involves disrupted neurosteroidogenesis and responds to allopregnanolone. Nat Med 10(7):704-711 (Pubitemid 38937635)
236. Haraguchi S, Hara S, Ubuka T, Mita M, Tsutsui K (2012) Possible role of pineal allopregnanolone in Purkinje cell survival. Proc Natl Acad Sci U S A 109(51):21110-21115
237. Takayama C, Inoue Y (2004) GABAergic signaling in the developing cerebellum. Anat Sci Int 79(3):124-136 (Pubitemid 39232241)
238. Ortinski PI, Lu C, Takagaki K, Fu Z, Vicini S (2004) Expression of distinct alpha subunits of GABAA receptor regulates inhibitory synaptic strength. J Neurophysiol 92(3):1718-1727 (Pubitemid 39100668)
239. Takayama C, Inoue Y (2004) Extrasynaptic localization of GABA in the developing mouse cerebellum. Neurosci Res 50(4):447-458 (Pubitemid 39572991)
240. Succol F, Fiumelli H, Benfenati F, Cancedda L, Barberis A (2012) Intracellular chloride concentration influences the GABAA receptor subunit composition. Nat Commun 3:738
241. Ortinski PI, Turner JR, Barberis A, Motamedi G, Yasuda RP, Wolfe BB, Kellar KJ, Vicini S (2006) Deletion of the GABA(A) receptor alpha1 subunit increases tonic GABA(A) receptor current: a role for GABA uptake transporters. J Neurosci 26(36):9323-9331 (Pubitemid 44359858)
242. - channels are highly permeable to HCO3. Am J Physiol Cell Physiol 294(6):C1371-C1377
243. Lee S, Yoon BE, Berglund K, Oh SJ, Park H, Shin HS, Augustine GJ, Lee CJ (2010) Channel-mediated tonic GABA release from glia. Science 330(6005):790-796
244. Buard I, Steinmetz CC, Claudepierre T, Pfrieger FW (2009) Glial cells promote dendrite formation and the reception of synaptic input in Purkinje cells from postnatal mice. Glia 58(5):538-545
245. Backman C, West JR, Mahoney JC, Palmer MR (1998) Electrophysiological characterization of cerebellar neurons from adult rats exposed to ethanol during development. Alcohol Clin Exp Res 22(5):1137-1145 (Pubitemid 28409009)
246. Bjorklund H, Palmer MR, Lind B, Hoffer BJ, Olson L (1983) Postnatal lead exposure alters spontaneous cerebellar Purkinje neuron discharge. Environ Res 31(2):448-459 (Pubitemid 13024078)
247. Dobbing J, Smart JL (1974) Vulnerability of developing brain and behaviour. Br Med Bull 30(2):164-168
248. Jones KL, Smith DW (1973) Recognition of the fetal alcohol syndrome in early infancy. Lancet 302(7836):999-1001
249. Jones KL, Smith DW, Ulleland CN, Streissguth P (1973) Pattern of malformation in offspring of chronic alcoholic mothers. Lancet 1(7815):1267-1271
250. Olney JW (2004) Fetal alcohol syndrome at the cellular level. Addict Biol 9(2):137-149, discussion 151
251. Medina AE (2011) Fetal alcohol spectrum disorders and abnormal neuronal plasticity. Neuroscientist 17(3):274-287
252. Clarren SK, Alvord EC Jr, Sumi SM, Streissguth AP, Smith DW (1978) Brain malformations related to prenatal exposure to ethanol. J Pediatr 92(1):64-67 (Pubitemid 8287927)
253. Liljelund P, Netzeband JG, Gruol DL (2000) L-type calcium channels mediate calcium oscillations in early postnatal Purkinje neurons. J Neurosci 20(19):7394-7403
254. Mody I (2008) Extrasynaptic GABAA receptors in the crosshairs of hormones and ethanol. Neurochem Int 52(1-2):60-64
255. Follesa P, Biggio F, Caria S, Gorini G, Biggio G (2004) Modulation of GABA(A) receptor gene expression by allopregnanolone and ethanol. Eur J Pharmacol 500(1-3):413-425 (Pubitemid 39304024)
256. Liang J, Suryanarayanan A, Abriam A, Snyder B, Olsen RW, Spigelman I (2007) Mechanisms of reversible GABAA receptor plasticity after ethanol intoxication. J Neurosci 27(45):12367-12377 (Pubitemid 350085483)
257. Uusi-Oukari M, Korpi ER (2010) Regulation of GABA(A) receptor subunit expression by pharmacological agents. Pharmacol Rev 62(1):97-135
258. Andang M, Hjerling-Leffler J, Moliner A, Lundgren TK, Castelo-Branco G, Nanou E, Pozas E, Bryja V, Halliez S, Nishimaru H, Wilbertz J, Arenas E, Koltzenburg M, Charnay P, El Manira A, Ibanez CF, Ernfors P (2008) Histone H2AX-dependent GABA(A) receptor regulation of stem cell proliferation. Nature 451(7177):460-464 (Pubitemid 351158886)
259. Rula EY, Lagrange AH, Jacobs MM, Hu N, Macdonald RL, Emeson RB (2008) Developmental modulation of GABA(A) receptor function by RNA editing. J Neurosci 28(24):6196-6201
260. Choi DS, Wei W, Deitchman JK, Kharazia VN, Lesscher HM, McMahon T, Wang D, Qi ZH, Sieghart W, Zhang C, Shokat KM, Mody I, Messing RO (2008) Protein kinase Cdelta regulates ethanol intoxication and enhancement of GABA-stimulated tonic current. J Neurosci 28(46):11890-11899
261. Nicolai J, Vles JS, Aldenkamp AP (2008) Neurodevelopmental delay in children exposed to antiepileptic drugs in utero: a critical review directed at structural study-bias. J Neurol Sci 271(1-2):1-14