GABAergic depolarization during early cortical development and implications for anticonvulsive therapy in neonates

Epilepsia

Volumn 52, Issue 9, 2011, Pages 1532-1543

  Kirmse, Knut ^a   Witte, Otto W ^a   Holthoff, Knut ^a  

^a JENA UNIVERSITY HOSPITAL   (Germany)

Author keywords

Bumetanide; Chloride; Cortex; Epilepsy; GABAA receptor; NKCC1

Indexed keywords

3 HYDROXYBUTYRIC ACID; 4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; ACETOACETIC ACID; ACETONE; ADENOSINE TRIPHOSPHATE; ANTICONVULSIVE AGENT; BARBITURIC ACID DERIVATIVE; BENZODIAZEPINE; BUMETANIDE; CALCIUM ION; CHLORINE; FATTY ACID; ION; LACTIC ACID; PHENOBARBITAL; POTASSIUM CHLORIDE COTRANSPORTER; PYRUVIC ACID; SODIUM POTASSIUM CHLORIDE COTRANSPORTER; VOLTAGE GATED CALCIUM CHANNEL; VOLTAGE GATED POTASSIUM CHANNEL; VOLTAGE GATED SODIUM CHANNEL;

ALLOSTERISM; ANTICONVULSANT ACTIVITY; ANTICONVULSANT THERAPY; ASTROCYTE; BRAIN CELL; BRAIN DEVELOPMENT; BRAIN FORNIX; BREAST MILK; CALCIUM CELL LEVEL; CELL POLARITY; DRUG EFFICACY; DRUG TARGETING; ENERGY METABOLISM; ENTORHINAL CORTEX; EXTRACELLULAR SPACE; GABAERGIC DEPOLARIZATION; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS; HOMEOSTASIS; HUMAN; HYPERPOLARIZATION; LIPID METABOLISM; NEOCORTEX; NERVE CELL EXCITABILITY; NERVE CELL MEMBRANE CONDUCTANCE; NERVE CELL MEMBRANE STEADY POTENTIAL; NERVE CELL STIMULATION; NEUROMODULATION; NEUROTRANSMISSION; NEWBORN DISEASE; NONHUMAN; OSMOREGULATION; POSTNATAL DEVELOPMENT; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR BLOCKING; REVIEW; SEIZURE; SYNAPSE; WESTERN BLOTTING;

ANIMALS; ANIMALS, NEWBORN; ANTICONVULSANTS; CEREBRAL CORTEX; DISEASE MODELS, ANIMAL; EPILEPSY; GAMMA-AMINOBUTYRIC ACID; HUMANS; INFANT, NEWBORN; MEMBRANE POTENTIALS; MODELS, BIOLOGICAL;

EID: 80052530373     PISSN: 00139580     EISSN: 15281167     Source Type: Journal    
DOI: 10.1111/j.1528-1167.2011.03128.x     Document Type: Review

References (118)

1. Achilles K, Okabe A, Ikeda M, Shimizu-Okabe C, Yamada J, Fukuda A, Luhmann HJ, Kilb W,. (2007) Kinetic properties of Cl uptake mediated by Na+-dependent K+-2Cl cotransport in immature rat neocortical neurons. J Neurosci 27: 8616-8627. (Pubitemid 47254259)
2. Allene C, Cattani A, Ackman JB, Bonifazi P, Aniksztejn L, Ben-Ari Y, Cossart R,. (2008) Sequential generation of two distinct synapse-driven network patterns in developing neocortex. J Neurosci 28: 12851-12863.
3. Balakrishnan V, Becker M, Lohrke S, Nothwang HG, Guresir E, Friauf E,. (2003) Expression and function of chloride transporters during development of inhibitory neurotransmission in the auditory brainstem. J Neurosci 23: 4134-4145. (Pubitemid 36958433)
4. Baram TZ, Snead OC III,. (1990) Bicuculline induced seizures in infant rats: ontogeny of behavioral and electrocortical phenomena. Brain Res Dev Brain Res 57: 291-295.
5. Barkis WB, Ford KJ, Feller MB,. (2010) Non-cell-autonomous factor induces the transition from excitatory to inhibitory GABA signaling in retina independent of activity. Proc Natl Acad Sci U S A 107: 22302-22307.
6. Ben-Ari Y, Holmes GL,. (2006) Effects of seizures on developmental processes in the immature brain. Lancet Neurol 5: 1055-1063. (Pubitemid 44709981)
7. Ben-Ari Y, Cherubini E, Corradetti R, Gaiarsa JL,. (1989) Giant synaptic potentials in immature rat CA3 hippocampal neurones. J Physiol 416: 303-325. (Pubitemid 19223216)
8. 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: 1215-1284. (Pubitemid 350041471)
9. Blaesse P, Airaksinen MS, Rivera C, Kaila K,. (2009) Cation-chloride cotransporters and neuronal function. Neuron 61: 820-838.
10. Blume HK, Garrison MM, Christakis DA,. (2009) Neonatal seizures: treatment and treatment variability in 31 United States pediatric hospitals. J Child Neurol 24: 148-154.
11. Booth D, Evans DJ,. (2004) Anticonvulsants for neonates with seizures. Cochrane Database Syst Rev 4: CD004218.
12. Brumback AC, Staley KJ,. (2008) Thermodynamic regulation of NKCC1-mediated Cl- cotransport underlies plasticity of GABA(A) signaling in neonatal neurons. J Neurosci 28: 1301-1312. (Pubitemid 351231517)
13. Brustein E, Marandi N, Kovalchuk Y, Drapeau P, Konnerth A,. (2003) "In vivo" monitoring of neuronal network activity in zebrafish by two-photon Ca(2+) imaging. Pflugers Arch 446: 766-773. (Pubitemid 37215013)
14. Cancedda L, Fiumelli H, Chen K, Poo MM,. (2007) Excitatory GABA action is essential for morphological maturation of cortical neurons in vivo. J Neurosci 27: 5224-5235. (Pubitemid 46741781)
15. Chavas J, Forero ME, Collin T, Llano I, Marty A,. (2004) Osmotic tension as a possible link between GABA(A) receptor activation and intracellular calcium elevation. Neuron 44: 701-713. (Pubitemid 39531233)
16. Clancy RR,. (2006) Summary proceedings from the neurology group on neonatal seizures. Pediatrics 117: S23-S27. (Pubitemid 46063168)
17. Dzhala VI, Staley KJ,. (2003) Excitatory actions of endogenously released GABA contribute to initiation of ictal epileptiform activity in the developing hippocampus. J Neurosci 23: 1840-1846. (Pubitemid 36314739)
18. Dzhala VI, Talos DM, Sdrulla DA, Brumback AC, Mathews GC, Benke TA, Delpire E, Jensen FE, Staley KJ,. (2005) NKCC1 transporter facilitates seizures in the developing brain. Nat Med 11: 1205-1213. (Pubitemid 43093668)
19. Dzhala VI, Brumback AC, Staley KJ,. (2008) Bumetanide enhances phenobarbital efficacy in a neonatal seizure model. Ann Neurol 63: 222-235. (Pubitemid 351355301)
20. Edwards DA, Shah HP, Cao W, Gravenstein N, Seubert CN, Martynyuk AE,. (2010) Bumetanide alleviates epileptogenic and neurotoxic effects of sevoflurane in neonatal rat brain. Anesthesiology 112: 567-575.
21. Flint AC, Dammerman RS, Kriegstein AR,. (1999) Endogenous activation of metabotropic glutamate receptors in neocortical development causes neuronal calcium oscillations. Proc Natl Acad Sci U S A 96: 12144-12149. (Pubitemid 29502872)
22. Gamba G,. (2005) Molecular physiology and pathophysiology of electroneutral cation-chloride cotransporters. Physiol Rev 85: 423-493. (Pubitemid 40404634)
23. Garaschuk O, Linn J, Eilers J, Konnerth A,. (2000) Large-scale oscillatory calcium waves in the immature cortex. Nat Neurosci 3: 452-459. (Pubitemid 30495626)
24. Ge S, Goh EL, Sailor KA, Kitabatake Y, Ming GL, Song H,. (2006) GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature 439: 589-593. (Pubitemid 43185382)
25. Glass HC, Glidden D, Jeremy RJ, Barkovich AJ, Ferriero DM, Miller SP,. (2009) Clinical neonatal seizures are independently associated with outcome in infants at risk for hypoxic-ischemic brain injury. J Pediatr 155: 318-323.
26. Glykys J, Dzhala VI, Kuchibhotla KV, Feng G, Kuner T, Augustine G, Bacskai BJ, Staley KJ,. (2009) Differences in cortical versus subcortical GABAergic signaling: a candidate mechanism of electroclinical uncoupling of neonatal seizures. Neuron 63: 657-672.
27. Goldberg EM, Jeong HY, Kruglikov I, Tremblay R, Lazarenko RM, Rudy B,. (2011) Rapid developmental maturation of neocortical FS cell intrinsic excitability. Cereb Cortex 21: 666-682.
28. Gonzalez-Islas C, Chub N, Wenner P,. (2009) NKCC1 and AE3 appear to accumulate chloride in embryonic motoneurons. J Neurophysiol 101: 507-518.
29. Gulledge AT, Stuart GJ,. (2003) Excitatory actions of GABA in the cortex. Neuron 37: 299-309. (Pubitemid 36143824)
30. Hebert SC, Mount DB, Gamba G,. (2004) Molecular physiology of cation-coupled Cl- cotransport: the SLC12 family. Pflugers Arch 447: 580-593. (Pubitemid 38241442)
31. Hennou S, Khalilov I, Diabira D, Ben-Ari Y, Gozlan H,. (2002) Early sequential formation of functional GABA(A) and glutamatergic synapses on CA1 interneurons of the rat foetal hippocampus. Eur J Neurosci 16: 197-208. (Pubitemid 36160240)
32. Holmgren CD, Mukhtarov M, Malkov AE, Popova IY, Bregestovski P, Zilberter Y,. (2010) Energy substrate availability as a determinant of neuronal resting potential, GABA signaling and spontaneous network activity in the neonatal cortex in vitro. J Neurochem 112: 900-912.
33. Holter NI, Zylla MM, Zuber N, Bruehl C, Draguhn A,. (2010) Tonic GABAergic control of mouse dentate granule cells during postnatal development. Eur J Neurosci 32: 1300-1309.
34. Holtkamp M, Meierkord H,. (2007) Anticonvulsant, antiepileptogenic, and antiictogenic pharmacostrategies. Cell Mol Life Sci 64: 2023-2041. (Pubitemid 47094429)
35. Hübner CA, Lorke DE, Hermans-Borgmeyer I,. (2001) Expression of the Na-K-2Cl-cotransporter NKCC1 during mouse development. Mech Dev 102: 267-269. (Pubitemid 32273612)
36. Irwin RP, Allen CN,. (2009) GABAergic signaling induces divergent neuronal Ca2+ responses in the suprachiasmatic nucleus network. Eur J Neurosci 30: 1462-1475.
37. Isaev D, Isaeva E, Khazipov R, Holmes GL,. (2005) Anticonvulsant action of GABA in the high potassium-low magnesium model of ictogenesis in the neonatal rat hippocampus in vivo and in vitro. J Neurophysiol 94: 2987-2992. (Pubitemid 41324713)
38. Javaheri S, Davis C, Rogers DH,. (1993) Ionic composition of cisternal CSF in acute respiratory acidosis: lack of effect of large dose bumetanide. J Neurochem 61: 1525-1529. (Pubitemid 23285113)
39. Jean-Xavier C, Mentis GZ, O'Donovan MJ, Cattaert D, Vinay L,. (2007) Dual personality of GABA/glycine-mediated depolarizations in immature spinal cord. Proc Natl Acad Sci U S A 104: 11477-11482. (Pubitemid 47175165)
40. Jensen FE,. (2009) Neonatal seizures: an update on mechanisms and management. Clin Perinatol 36: 881-900, vii.
41. Kahle KT, Staley KJ,. (2008) The bumetanide-sensitive Na-K-2Cl cotransporter NKCC1 as a potential target of a novel mechanism-based treatment strategy for neonatal seizures. Neurosurg Focus 25: E22.
42. Kahle KT, Staley KJ, Nahed BV, Gamba G, Hebert SC, Lifton RP, Mount DB,. (2008) Roles of the cation-chloride cotransporters in neurological disease. Nat Clin Pract Neurol 4: 490-503.
43. Kahle KT, Barnett SM, Sassower KC, Staley KJ,. (2009) Decreased seizure activity in a human neonate treated with bumetanide, an inhibitor of the Na(+)-K(+)-2Cl(-) cotransporter NKCC1. J Child Neurol 24: 572-576.
44. Katz LC, Shatz CJ,. (1996) Synaptic activity and the construction of cortical circuits. Science 274: 1133-1138. (Pubitemid 26389269)
45. Khazipov R, Luhmann HJ,. (2006) Early patterns of electrical activity in the developing cerebral cortex of humans and rodents. Trends Neurosci 29: 414-418. (Pubitemid 44108244)
46. Kilb W, Sinning A, Luhmann HJ,. (2007) Model-specific effects of bumetanide on epileptiform activity in the in-vitro intact hippocampus of the newborn mouse. Neuropharmacology 53: 524-533. (Pubitemid 47284187)
47. Kirmse K, Kirischuk S,. (2006) Ambient GABA constrains the strength of GABAergic synapses at Cajal-Retzius cells in the developing visual cortex. J Neurosci 26: 4216-4227. (Pubitemid 44315381)
48. Kirmse K, Dvorzhak A, Kirischuk S, Grantyn R,. (2008) GABA transporter 1 tunes GABAergic synaptic transmission at output neurons of the mouse neostriatum. J Physiol 586: 5665-5678.
49. Kirmse K, Witte OW, Holthoff K,. (2010) GABA depolarizes immature neocortical neurons in the presence of the ketone body β-hydroxybutyrate. J Neurosci 30: 16002-16007.
50. 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. (Pubitemid 27111107)
51. Leinekugel X, Khazipov R, Cannon R, Hirase H, Ben-Ari Y, Buzsaki G,. (2002) Correlated bursts of activity in the neonatal hippocampus in vivo. Science 296: 2049-2052. (Pubitemid 34627532)
52. Li H, Tornberg J, Kaila K, Airaksinen MS, Rivera C,. (2002) Patterns of cation-chloride cotransporter expression during embryonic rodent CNS development. Eur J Neurosci 16: 2358-2370. (Pubitemid 36056960)
53. Luhmann HJ, Prince DA,. (1991) Postnatal maturation of the GABAergic system in rat neocortex. J Neurophysiol 65: 247-263.
54. Macdonald RL, Olsen RW,. (1994) GABAA receptor channels. Annu Rev Neurosci 17: 569-602. (Pubitemid 2067782)
55. MacDonald RL, Rogers CJ, Twyman RE,. (1989) Barbiturate regulation of kinetic properties of the GABAA receptor channel of mouse spinal neurones in culture. J Physiol 417: 483-500. (Pubitemid 19250817)
56. MacVicar BA, Feighan D, Brown A, Ransom B,. (2002) Intrinsic optical signals in the rat optic nerve: role for K(+) uptake via NKCC1 and swelling of astrocytes. Glia 37: 114-123. (Pubitemid 34161542)
57. Marandi N, Konnerth A, Garaschuk O,. (2002) Two-photon chloride imaging in neurons of brain slices. Pflugers Arch 445: 357-365. (Pubitemid 35447500)
58. Mares P,. (2009) Age- and dose-specific anticonvulsant action of bumetanide in immature rats. Physiol Res 58: 927-930.
59. Mazarati A, Shin D, Sankar R,. (2009) Bumetanide inhibits rapid kindling in neonatal rats. Epilepsia 50: 2117-2122.
60. Mienville JM,. (1998) Persistent depolarizing action of GABA in rat Cajal-Retzius cells. J Physiol 512 (Pt 3): 809-817.
61. Milh M, Kaminska A, Huon C, Lapillonne A, Ben-Ari Y, Khazipov R,. (2007) Rapid cortical oscillations and early motor activity in premature human neonate. Cereb Cortex 17: 1582-1594.
62. Minlebaev M, Khazipov R,. (2011) Antiepileptic effects of endogenous beta-hydroxybutyrate in suckling infant rats. Epilepsy Res doi:.
63. Minlebaev M, Ben-Ari Y, Khazipov R,. (2007) Network mechanisms of spindle-burst oscillations in the neonatal rat barrel cortex in vivo. J Neurophysiol 97: 692-700. (Pubitemid 46150789)
64. Morita K, Tsumoto K, Aihara K,. (2005) Possible effects of depolarizing GABAA conductance on the neuronal input-output relationship: a modeling study. J Neurophysiol 93: 3504-3523. (Pubitemid 40720925)
65. Morita K, Tsumoto K, Aihara K,. (2006) Bidirectional modulation of neuronal responses by depolarizing GABAergic inputs. Biophys J 90: 1925-1938.
66. Mueller AL, Taube JS, Schwartzkroin PA,. (1984) Development of hyperpolarizing inhibitory postsynaptic potentials and hyperpolarizing response to gamma-aminobutyric acid in rabbit hippocampus studied in vitro. J Neurosci 4: 860-867. (Pubitemid 14127196)
67. Mukhtarov M, Ivanov A, Zilberter Y, Bregestovski P,. (2010) Inhibition of spontaneous network activity in neonatal hippocampal slices by energy substrates is not correlated with intracellular acidification. J Neurochem 116: 316-321.
68. Nardou R, Ben-Ari Y, Khalilov I,. (2009) Bumetanide, an NKCC1 antagonist, does not prevent formation of epileptogenic focus but blocks epileptic focus seizures in immature rat hippocampus. J Neurophysiol 101: 2878-2888.
69. Nardou R, Yamamoto S, Chazal G, Bhar A, Ferrand N, Dulac O, Ben-Ari Y, Khalilov I,. (2011) Neuronal chloride accumulation and excitatory GABA underlie aggravation of neonatal epileptiform activities by phenobarbital. Brain 134: 987-1002.
70. Ostby I, Oyehaug L, Einevoll GT, Nagelhus EA, Plahte E, Zeuthen T, Lloyd CM, Ottersen OP, Omholt SW,. (2009) Astrocytic mechanisms explaining neural-activity-induced shrinkage of extraneuronal space. PLoS Comput Biol 5: e1000272.
71. 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: 6414-6423. (Pubitemid 26337365)
72. Owens DF, Liu X, Kriegstein AR,. (1999) Changing properties of GABA(A) receptor-mediated signaling during early neocortical development. J Neurophysiol 82: 570-583. (Pubitemid 29387834)
73. Painter MJ, Scher MS, Stein AD, Armatti S, Wang Z, Gardiner JC, Paneth N, Minnigh B, Alvin J,. (1999) Phenobarbital compared with phenytoin for the treatment of neonatal seizures. N Engl J Med 341: 485-489. (Pubitemid 29372888)
74. Payne JA, Rivera C, Voipio J, Kaila K,. (2003) Cation-chloride co-transporters in neuronal communication, development and trauma. Trends Neurosci 26: 199-206. (Pubitemid 36412002)
75. Pfeffer CK, Stein V, Keating DJ, Maier H, Rinke I, Rudhard Y, Hentschke M, Rune GM, Jentsch TJ, Hübner CA,. (2009) NKCC1-dependent GABAergic excitation drives synaptic network maturation during early hippocampal development. J Neurosci 29: 3419-3430.
76. Purpura DP, Prelevic S, Santini M,. (1968) Postsynaptic potentials and spike variations in the feline hippocampus during postnatal ontogenesis. Exp Neurol 22: 408-422.
77. Reynolds A, Brustein E, Liao M, Mercado A, Babilonia E, Mount DB, Drapeau P,. (2008) Neurogenic role of the depolarizing chloride gradient revealed by global overexpression of KCC2 from the onset of development. J Neurosci 28: 1588-1597. (Pubitemid 351287036)
78. Rheims S, Minlebaev M, Ivanov A, Represa A, Khazipov R, Holmes GL, Ben-Ari Y, Zilberter Y,. (2008a) Excitatory GABA in rodent developing neocortex in vitro. J Neurophysiol 100: 609-619.
79. Rheims S, Represa A, Ben-Ari Y, Zilberter Y,. (2008b) Layer-specific generation and propagation of seizures in slices of developing neocortex: role of excitatory GABAergic synapses. J Neurophysiol 100: 620-628.
80. Rheims S, Holmgren CD, Chazal G, Mulder J, Harkany T, Zilberter T, Zilberter Y,. (2009) GABA action in immature neocortical neurons directly depends on the availability of ketone bodies. J Neurochem 110: 1330-1338.
81. Richter D, Luhmann HJ, Kilb W,. (2010) Intrinsic activation of GABA(A) receptors suppresses epileptiform activity in the cerebral cortex of immature mice. Epilepsia 51: 1483-1492.
82. 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.
83. Rivera C, Voipio J, Kaila K,. (2005) Two developmental switches in GABAergic signalling: the K+-Cl- cotransporter KCC2 and carbonic anhydrase CAVII. J Physiol 562: 27-36. (Pubitemid 40207781)
84. Romijn HJ, Hofman MA, Gramsbergen A,. (1991) At what age is the developing cerebral cortex of the rat comparable to that of the full-term newborn human baby? Early Hum Dev 26: 61-67.
85. Ruusuvuori E, Kirilkin I, Pandya N, Kaila K,. (2010) Spontaneous network events driven by depolarizing GABA action in neonatal hippocampal slices are not attributable to deficient mitochondrial energy metabolism. J Neurosci 30: 15638-15642.
86. Sakata Y, Fujioka T, Endoh H, Nakamura S,. (2006) In vivo optical recordings of synaptic transmission and intracellular Ca2+ and Cl- in the superior colliculus of fetal rats. Eur J Neurosci 23: 1405-1416.
87. Sankar R, Painter MJ,. (2005) Neonatal seizures: after all these years we still love what doesn't work. Neurology 64: 776-777. (Pubitemid 40316310)
88. Sankar R, Rho JM,. (2007) Do seizures affect the developing brain? Lessons from the laboratory. J Child Neurol 22: 21S-29S. (Pubitemid 46938996)
89. Schwartzkroin PA, Baraban SC, Hochman DW,. (1998) Osmolarity, ionic flux, and changes in brain excitability. Epilepsy Res 32: 275-285. (Pubitemid 28419496)
90. Shimizu-Okabe C, Yokokura M, Okabe A, Ikeda M, Sato K, Kilb W, Luhmann HJ, Fukuda A,. (2002) Layer-specific expression of Cl- transporters and differential [Cl-]i in newborn rat cortex. Neuroreport 13: 2433-2437. (Pubitemid 36143539)
91. Sipila ST, Schuchmann S, Voipio J, Yamada J, Kaila K,. (2006) The cation-chloride cotransporter NKCC1 promotes sharp waves in the neonatal rat hippocampus. J Physiol 573: 765-773. (Pubitemid 43852771)
92. Sipila ST, Huttu K, Yamada J, Afzalov R, Voipio J, Blaesse P, Kaila K,. (2009) Compensatory enhancement of intrinsic spiking upon NKCC1 disruption in neonatal hippocampus. J Neurosci 29: 6982-6988.
93. Staley K,. (1992) Enhancement of the excitatory actions of GABA by barbiturates and benzodiazepines. Neurosci Lett 146: 105-107.
94. Stein V, Hermans-Borgmeyer I, Jentsch TJ, Hübner CA,. (2004) Expression of the KCl cotransporter KCC2 parallels neuronal maturation and the emergence of low intracellular chloride. J Comp Neurol 468: 57-64. (Pubitemid 37531643)
95. Study RE, Barker JL,. (1981) Diazepam and ( - )-pentobarbital: fluctuation analysis reveals different mechanisms for potentiation of gamma-aminobutyric acid responses in cultured central neurons. Proc Natl Acad Sci U S A 78: 7180-7184.
96. Sung KW, Kirby M, McDonald MP, Lovinger DM, Delpire E,. (2000) Abnormal GABAA receptor-mediated currents in dorsal root ganglion neurons isolated from Na-K-2Cl cotransporter null mice. J Neurosci 20: 7531-7538.
97. Sykova E,. (2004) Extrasynaptic volume transmission and diffusion parameters of the extracellular space. Neuroscience 129: 861-876. (Pubitemid 39556240)
98. Szabadics J, Varga C, Molnar G, Olah S, Barzo P, Tamas G,. (2006) Excitatory effect of GABAergic axo-axonic cells in cortical microcircuits. Science 311: 233-235. (Pubitemid 43108189)
99. Twyman RE, Rogers CJ, Macdonald RL,. (1989) Differential regulation of gamma-aminobutyric acid receptor channels by diazepam and phenobarbital. Ann Neurol 25: 213-220. (Pubitemid 19085510)
100. Tyzio R, Represa A, Jorquera I, Ben-Ari Y, Gozlan H, Aniksztejn L,. (1999) The establishment of GABAergic and glutamatergic synapses on CA1 pyramidal neurons is sequential and correlates with the development of the apical dendrite. J Neurosci 19: 10372-10382. (Pubitemid 30228044)
101. Tyzio R, Ivanov A, Bernard C, Holmes GL, Ben-Ari Y, Khazipov R,. (2003) Membrane potential of CA3 hippocampal pyramidal cells during postnatal development. J Neurophysiol 90: 2964-2972. (Pubitemid 37429997)
102. Tyzio R, Cossart R, Khalilov I, Minlebaev M, Hübner 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: 1788-1792. (Pubitemid 44969093)
103. Tyzio R, Allene C, Nardou R, Picardo MA, Yamamoto S, Sivakumaran S, Caiati MD, Rheims S, Minlebaev M, Milh M, Ferre P, Khazipov R, Romette JL, Lorquin J, Cossart R, Khalilov I, Nehlig A, Cherubini E, Ben-Ari Y,. (2011) Depolarizing actions of GABA in immature neurons depend neither on ketone bodies nor on pyruvate. J Neurosci 31: 34-45.
104. Vanhatalo S, Hellstrom-Westas L, De Vries LS,. (2009) Bumetanide for neonatal seizures: based on evidence or enthusiasm? Epilepsia 50: 1292-1293.
105. Vento M, de Vries LS, Alberola A, Blennow M, Steggerda S, Greisen G, Boronat N,. (2009) Approach to seizures in the neonatal period: a European perspective. Acta Paediatr 99: 497-501.
106. Verheugen JA, Fricker D, Miles R,. (1999) Noninvasive measurements of the membrane potential and GABAergic action in hippocampal interneurons. J Neurosci 19: 2546-2555. (Pubitemid 29162403)
107. Wahab A, Albus K, Heinemann U,. (2010) Age- and region-specific effects of anticonvulsants and bumetanide on 4-aminopyridine-induced seizure-like events in immature rat hippocampal-entorhinal cortex slices. Epilepsia 52: 94-103.
108. Wang DD, Kriegstein AR,. (2008) GABA regulates excitatory synapse formation in the neocortex via NMDA receptor activation. J Neurosci 28: 5547-5558.
109. Wang DD, Kriegstein AR,. (2010) Blocking early GABA depolarization with bumetanide results in permanent alterations in cortical circuits and sensorimotor gating deficits. Cereb Cortex 21: 574-587.
110. Wang DD, Krueger DD, Bordey A,. (2003) GABA depolarizes neuronal progenitors of the postnatal subventricular zone via GABAA receptor activation. J Physiol 550: 785-800. (Pubitemid 37010063)
111. Wells JE, Porter JT, Agmon A,. (2000) GABAergic inhibition suppresses paroxysmal network activity in the neonatal rodent hippocampus and neocortex. J Neurosci 20: 8822-8830.
112. Wheless JW, Clarke DF, Arzimanoglou A, Carpenter D,. (2007) Treatment of pediatric epilepsy: European expert opinion, 2007. Epileptic Disord 9: 353-412. (Pubitemid 351147653)
113. Wirrell EC,. (2005) Neonatal seizures: to treat or not to treat? Semin Pediatr Neurol 12: 97-105. (Pubitemid 40967987)
114. Woodruff A, Xu Q, Anderson SA, Yuste R,. (2009) Depolarizing effect of neocortical chandelier neurons. Front Neural Circuits 3: 15.
115. Yamada J, Okabe A, Toyoda H, Kilb W, Luhmann HJ, Fukuda A,. (2004) Cl- uptake promoting depolarizing GABA actions in immature rat neocortical neurones is mediated by NKCC1. J Physiol 557: 829-841. (Pubitemid 38961620)
116. Yuste R, Katz LC,. (1991) Control of postsynaptic Ca2+ influx in developing neocortex by excitatory and inhibitory neurotransmitters. Neuron 6: 333-344.
117. Zhang LL, Delpire E, Vardi N,. (2007) NKCC1 does not accumulate chloride in developing retinal neurons. J Neurophysiol 98: 266-277. (Pubitemid 47084818)
118. Zhu L, Polley N, Mathews GC, Delpire E,. (2008) NKCC1 and KCC2 prevent hyperexcitability in the mouse hippocampus. Epilepsy Res 79: 201-212.