Excitatory GABA in rodent developing neocortex in vitro

Journal of Neurophysiology

Volumn 100, Issue 2, 2008, Pages 609-619

  Rheims, Sylvain ^a   Minlebaev, Marat ^a   Ivanov, Anton ^a   Represa, Alfonso ^a   Khazipov, Rustem ^a   Holmes, Gregory L ^b   Ben Ari, Yehezkel ^a   Zilberter, Yuri ^a  

^a INSERM   (France)

^b DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; BUMETANIDE; N METHYL DEXTRO ASPARTIC ACID; 2 AMINO 5 PHOSPHOPENTANOIC ACID; 2,3 DIOXO 6 NITRO 7 SULFAMOYLBENZO(F)QUINOXALINE; 2,3-DIOXO-6-NITRO-7-SULFAMOYLBENZO(F)QUINOXALINE; 2-AMINO-5-PHOSPHOPENTANOIC ACID; AMINO ACID RECEPTOR BLOCKING AGENT; BIOCYTIN; DRUG DERIVATIVE; GABAERGIC RECEPTOR AFFECTING AGENT; LOOP DIURETIC AGENT; LYSINE; QUINOXALINE DERIVATIVE; VALINE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; BRAIN SLICE; CONTROLLED STUDY; DEPOLARIZATION; FEMALE; GABAERGIC TRANSMISSION; HYPERPOLARIZATION; IN VITRO STUDY; INTERNEURON; MALE; MEMBRANE DEPOLARIZATION; MEMBRANE STEADY POTENTIAL; NEOCORTEX; NERVE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SYNAPTIC TRANSMISSION; AGE; ANIMAL; BIOLOGICAL MODEL; CELL MEMBRANE POTENTIAL; CLASSIFICATION; CYTOLOGY; DRUG EFFECT; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOUSE; NEWBORN; PATCH CLAMP; PHYSIOLOGY;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; BUMETANIDE; EXCITATORY AMINO ACID ANTAGONISTS; FEMALE; GABA AGENTS; GAMMA-AMINOBUTYRIC ACID; INTERNEURONS; LYSINE; MALE; MEMBRANE POTENTIALS; MICE; MODELS, NEUROLOGICAL; NEOCORTEX; PATCH-CLAMP TECHNIQUES; PYRAMIDAL CELLS; QUINOXALINES; SODIUM POTASSIUM CHLORIDE SYMPORTER INHIBITORS; VALINE;

EID: 55249093849     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.90402.2008     Document Type: Article

References (57)

1. Adelsberger H, Garaschuk O, Konnerth A. Cortical calcium waves in resting newborn mice. Nat Neurosci 8: 988-990, 2005.
2. Adragna NC, Di Fulvio M, Lauf PK. Regulation of K-Cl cotransport: from function to genes. J Membr Biol 201: 109-137, 2004.
3. Agmon A, Connors BW. Thalamocortical responses of mouse somatosensory (barrel) cortex in vitro. Neuroscience 41: 365-380, 1991.
4. Aguilo A, Schwartz TH, Kumar VS, Peterlin ZA, Tsiola A, Soriano E, Yuste R. Involvement of cajal-retzius neurons in spontaneous correlated activity of embryonic and postnatal layer 1 from wild-type and reeler mice. J Neurosci 19: 10856-10868, 1999.
5. Ben-Ari Y. Excitatory actions of gaba during development: the nature of the nurture. Nat Rev Neurosci 3: 728-739, 2002.
6. Ben-Ari Y. Basic developmental rules and their implications for epilepsy in the immature brain. Epileptic Disord 8: 91-102, 2006.
7. Ben-Ari Y, Cherubini E, Corradetti R, Gaiarsa JL. Giant synaptic potentials in immature rat CA3 hippocampal neurones. J Physiol 416: 303-325, 1989.
8. Ben-Ari Y, Gaiarsa JL, Tyzio R, Khazipov R. GABA: a pioneer transmitter that excites immature neurons and generates primitive oscillations. Physiol Rev 87: 1215-1284, 2007.
9. Brumback AC, Staley KJ. Thermodynamic regulation of NKCC1-mediated Cl- cotransport underlies plasticity of GABA(A) signaling in neonatal neurons. J Neurosci 28: 1301-1312, 2008.
10. Burgard EC, Hablitz JJ. Developmental changes in NMDA and non-NMDA receptor-mediated synaptic potentials in rat neocortex. J Neurophysiol 69: 230-240, 1993.
11. Cang J, Renteria RC, Kaneko M, Liu X, Copenhagen DR, Stryker MP. Development of precise maps in visual cortex requires patterned spontaneous activity in the retina. Neuron 48: 797-809, 2005.
12. Corlew R, Bosma MM, Moody WJ. Spontaneous, synchronous electrical activity in neonatal mouse cortical neurones. J Physiol 560: 377-390, 2004.
13. Crepel V, Aronov D, Jorquera I, Represa A, Ben-Ari Y, Cossart R. A parturition-associated nonsynaptic coherent activity pattern in the developing hippocampus. Neuron 54: 105-120, 2007.
14. Cruikshank SJ, Rose HJ, Metherate R. Auditory thalamocortical synaptic transmission in vitro. J Neurophysiol 87: 361-384, 2002.
15. Davies CH, Davies SN, Collingridge GL. Paired-pulse depression of monosynaptic GABA-mediated inhibitory postsynaptic responses in rat hippocampus. J Physiol 424: 513-531, 1990.
16. Daw MI, Scott HL, Isaac JT. Developmental synaptic plasticity at the thalamocortical input to barrel cortex: mechanisms and roles. Mol Cell Neurosci 34: 493-502, 2007a.
17. Daw NW, Ashby MC, Isaac JTR. Coordinated developmental recruitment of latent fast spiking interneurons in layer IV barrel cortex. Nat Neurosci 10: 453-461, 2007b.
18. Dupont E, Hanganu IL, Kilb W, Hirsch S, Luhmann HJ. Rapid developmental switch in the mechanisms driving early cortical columnar networks. Nature 439: 79-83, 2006.
19. Dzhala VI, Talos DM, Sdrulla DA, Brumback AC, Mathews GC, Benke TA, Delpire E, Jensen FE, Staley KJ. NKCC1 transporter facilitates seizures in the developing brain. Nat Med 11: 1205-1213, 2005.
20. Feller MB. Spontaneous correlated activity in developing neural circuits. Neuron 22: 653-656, 1999.
21. Franceschetti S, Sancini G, Panzica F, Radici C, Avanzini G. Postnatal differentiation of firing properties and morphological characteristics in layer V pyramidal neurons of the sensorimotor cortex. Neuroscience 83: 1013-1024, 1998.
22. Galli L, Maffei L. Spontaneous impulse activity of rat retinal ganglion cells in prenatal life. Science 242: 90-91, 1988.
23. Garaschuk O, Linn J, Eilers J, Konnerth A. Large-scale oscillatory calcium waves in the immature cortex. Nat Neurosci 3: 452-459, 2000.
24. Hanganu IL, Ben-Ari Y, Khazipov R. Retinal waves trigger spindle bursts in the neonatal rat visual cortex. J Neurosci 26: 6728-6736, 2006.
25. Hannaert P, Alvarez-Guerra M, Pirot D, Nazaret C, Garay RP. Rat NKCC2/NKCC1 cotransporter selectivity for loop diuretic drugs. Naunyn Schmiedebergs Arch Pharmacol 365: 193-199, 2002.
26. Häusser M, Major G, Stuart G. Differential shunting of EPSPs by action potentials. Science 291: 138-141, 2001.
27. Kandler K, Gillespie DC. Developmental refinement of inhibitory soundlocalization circuits. Trends Neurosci 28: 290-296, 2005.
28. Katz LC, Shatz CJ. Synaptic activity and the construction of cortical circuits. Science 274: 1133-1138, 1996.
29. Khazipov R, Esclapez M, Caillard O, Bernard C, Khalilov I, Tyzio R, Hirsch J, Dzhala V, Berger B, Ben-Ari Y. Early development of neuronal activity in the primate hippocampus in utero. J Neurosci 21: 9770-9781, 2001.
30. Khazipov R, Khalilov I, Tyzio R, Morozova E, Ben-Ari Y, Holmes GL. Developmental changes in GABAergic actions and seizure susceptibility in the rat hippocampus. Eur J Neurosci 19: 590-600, 2004a.
31. Khazipov R, Sirote A, Leinekugel X, Holmes GL, Ben-Ari Y, Buzsaki G. Early motor activity drives spindle bursts in the developing somatosensory cortex. Nature 432: 758-761, 2004b.
32. Lee CM, Chang WC, Chang KB, Shyu BC. Synaptic organization and input-specific short-term plasticity in anterior cingulate cortical neurons with intact thalamic inputs. Eur J Neurosci 25: 2847-2861, 2007.
33. Luhmann HJ, Prince DA. Postnatal maturation of the GABAergic system in rat neocortex. J Neurophysiol 65: 247-263, 1991.
34. MacLean JN, Fenstermaker V, Watson BO, Yuste R. A visual thalamocortical slice. Nat Methods 3: 129-134, 2006.
35. McCabe AK, Chisholm SL, Picken-Bahrey HL, Moody WJ. The self-regulating nature of spontaneous synchronized activity in developing mouse cortical neurones. J Physiol 577: 155-167, 2006.
36. McCormick DA, Prince DA. Post-natal development of electrophysiological properties of rat cerebral cortical pyramidal neurones. J Physiol 393: 743-762, 1987.
37. Meister M, Wong RO, Baylor DA, Shatz CJ. Synchronous bursts of action potentials in ganglion cells of the developing mammalian retina. Science 252: 939-943, 1991.
38. Milh M, Kaminska A, Huon C, Lapillonne A, Ben-Ari Y, Khazipov R. Rapid cortical oscillations and early motor activity in premature human neonate. Cereb Cortex 17: 1582-1594, 2007.
39. Minlebaev M, Ben-Ari Y, Khazipov R. Network mechanisms of spindle-burst oscillations in the neonatal rat barrel cortex in vivo. J Neurophysiol 97: 692-700, 2006.
40. Moody WJ, Bosma MM. Ion channel development, spontaneous activity, and activity-dependent development in nerve and muscle cells. Physiol Rev 85: 883-941, 2005.
41. Owens DF, Boyce LH, Davies CH, Kriegstein AR. Excitatory GABA responses in embryonic and neonatal cortical slices demonstrated by gramicidin perforated-patch recordings and calcium imaging. J Neurosci 16: 6414-6423, 1996.
42. Owens DF, Kriegstein AR. Patterns of intracellular calcium fluctuation in precursor cells of the neocortical ventricular zone. J Neurosci 18: 5374-5388, 1998.
43. Owens DF, Liu X, Kriegstein AR. Changing properties of GABAA receptor-mediated signaling during early neocortical development. J Neurophysiol 82: 570-583, 1999.
44. Payne JA, Rivera C, Voipio J, Kaila K. Cation-chloride co-transporters in neuronal communication, development and trauma. Trends Neurosci 26: 199-206, 2003.
45. Picken Bahrey HL, Moody WJ. Early development of voltage-gated ion currents and firing properties in neurons of the mouse cerebral cortex. J Neurophysiol 89: 1761-1773, 2003.
46. Reboreda A, Raouf R, Alonso A, Seguela P. Development of cholinergic modulation and graded persistent activity in layer v of medial entorhinal cortex. J Neurophysiol 97: 3937-3947, 2007.
47. Rheims S, Represa A, Ben-Ari Y, Zilberter Y. Layer-specific generation and propagation of seizures in slices of developing neocortex: role of excitatory GABAergic synapses. J Neurophysiol doi:10.1152/jn.90403. 2008.
48. Salin PA, Prince DA. Spontaneous GABAA receptor-mediated inhibitory currents in adult rat somatosensory cortex. J Neurophysiol 75: 1573-1588, 1996.
49. Tyzio R, Cossart R, Khalilov I, Minlebaev M, Hubner CA, Represa A, Ben-Ari Y, Khazipov R. Maternal oxytocin triggers a transient inhibitory switch in GABA signaling in the fetal brain during delivery. Science 314: 1788-1792, 2006.
50. Tyzio R, Ivanov A, Bernard C, Holmes GL, Ben-Ari Y, Khazipov R. Membrane potential of CA3 hippocampal pyramidal cells during postnatal development. J Neurophysiol 90: 2964-2972, 2003.
51. Tyzio R, Minlebaev M, Rheims S, Ivanov A, Jorquera I, Holmes GL, Zilberter Y, Ben-Ari Y, Khazipov R. Postnatal change in somatic GABA signaling in the rat hippocampus. Eur J Neurosci 27: 2515-2528, 2008.
52. Williams SR, Stuart GJ. Voltage- and site-dependent control of the somatic impact of dendritic IPSPs. J Neurosci 23: 7358-7367, 2003.
53. Yamada J, Furukawa T, Ueno S, Yamamoto S, Fukuda A. Molecular basis for the GABAA receptor-mediated tonic inhibition in rat somatosensory cortex. Cereb Cortex 17: 1782-1787, 2007.
54. Yamada KA, Okabe A, Toyoda H, Kilb W, Luhmann HJ, Fukuda A. Cl- uptake promoting depolarizing GABA actions inimmature rat neocortical neurones is mediated by NKCC1. J Physiol (Lond) 557: 829-841, 2004.
55. Yuste R, Peinado A, Katz LC. Neuronal domains in developing neocortex. Science 257: 665-669, 1992.
56. Zhang ZW. Maturation of layer V pyramidal neurons in the rat prefrontal cortex: intrinsic properties and synaptic function. J Neurophysiol 91: 1171-1182, 2004.
57. Zhou FM, Hablitz JJ. Postnatal development of membrane properties of layer I neurons in rat neocortex. J Neurosci 16: 1131-1139, 1996.