Spontaneous network events driven by depolarizing GABA action in neonatal hippocampal slices are not attributable to deficient mitochondrial energy metabolism

Journal of Neuroscience

Volumn 30, Issue 46, 2010, Pages 15638-15642

  Ruusuvuori, Eva ^a   Kirilkin, Ilya ^a   Pandya, Nikhil ^a   Kaila, Kai ^a,b  

^a Department of Biosciences ^*  (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; GLUCOSE; LACTIC ACID; PROPIONIC ACID;

ANIMAL TISSUE; ARTICLE; CELL PH; ENERGY METABOLISM; HIPPOCAMPUS; MEMBRANE DEPOLARIZATION; METABOLIC DISORDER; MITOCHONDRIAL MEMBRANE POTENTIAL; NEWBORN; NONHUMAN; PRIORITY JOURNAL; RAT;

ACTION POTENTIALS; ANIMALS; ANIMALS, NEWBORN; ENERGY METABOLISM; GAMMA-AMINOBUTYRIC ACID; GLUCOSE; HIPPOCAMPUS; LACTIC ACID; MITOCHONDRIA; NERVE NET; RATS; RATS, WISTAR;

EID: 78449251558     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3355-10.2010     Document Type: Article

References (32)

1. Ben-Ari Y, Cherubini E, Corradetti R, Gaiarsa JL (1989) Giant synaptic potentials in immature rat CA3 hippocampal neurons. J Physiol 416: 303-325. (Pubitemid 19223216)
2. 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)
3. Blaesse P, Airaksinen MS, Rivera C, Kaila K (2009) Cation-chloride cotransporters and neuronal function. Neuron 61:820-838.
4. Cherubini E, Gaiarsa JL, Ben-Ari Y (1991) GABA: an excitatory transmitter in early postnatal life. Trends Neurosci 14:515-519.
5. Chesler M (2003) Regulation and modulation of pH in the brain. Physiol Rev 83:1183-1221.
6. Duchen MR (1992) Ca2+-dependent changes in the mitochondrila energetics in single dissociated mouse sensory neurons. Biochem J 283:41-50.
7. Dulla CG, Dobelis P, Pearson T, Frenguelli BG, Staley KJ, Masino SA (2005) Adenosine and ATP link P-CO2 to cortical excitability via pH. Neuron 48:1011-1023. (Pubitemid 41814704)
8. Dulla CG, Frenguelli BG, Staley KJ, Masino SA (2009) Intracellular acidification causes adenosine release during states of hyperexcitability in the hippocampus. J Neurophysiol 102:1984-1993.
9. 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.
10. Enyedi P, Czirják G (2010) Molecular background of leak K+ currents: two-pore domain potassium channels. Physiol Rev 90:559-605.
11. Erecinska M, Cherian S, Silver IA (2004) Energy metabolism in mammalian brain during development. Prog Neurobiol 73:397-445. (Pubitemid 39099270)
12. Gibbs ME, Hertz L (2008) Inhibition of astrocytic energy metabolism by D-lactate exposure impairs memory. Neurochem Int 52:1012-1018.
13. Helmy M, Tolner EA, Vanhatalo S, Voipio J, Kaila K (2010) Brain alkalosis causes birth asphyxia seizures suggesting a novel therapeutic strategy. Ann Neurol, in press.
14. 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.
15. Kaila K, Ransom BR (1998) pH and brain function. New York: Wiley.
16. Mason MJ, Mattsson K, Pasternack M, Voipio J, Kaila K (1990) Postsynaptic fall in intracellular pH and increase in surface pH caused by efflux of formate and acetate anions through GABA-gated channels in crayfish muscle fibres. Neuroscience 34:359-368.
17. Nguyen NH, Morland C, Gonzalez SV, Rise F, Storm-Mathisen J, Gundersen V, Hassel B (2007) Propionate increases neuronal histone acetylation, but is metabolized oxidatively by glia: relevance for propionic acidemia. J Neurochem 101:806-814.
18. Ortsäter H, Liss P, Akerman KE, Bergsten P (2002) Contribution of glycolytic and mitochondrial pathways in glucose-induced changes in islet respiration and insulin secretion. Pflugers Arch 444:506-512. (Pubitemid 35469114)
19. Poole RC, Halestrap AP (1993) Transport of lactate and other monocarboxylates across mammalian plasma membranes. Am J Physiol 264: C761-C782.
20. Raichle ME, Mintun MA (2006) Brain work and brain imaging. Annu Rev Neurosci 29:449-476.
21. 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.
22. Roos A, Boron WF (1981) Intracellular pH. Physiol Rev 61:296-434.
23. Ros J, Pecinska N, Alessandri B, Landolt H, Fillenz M (2001) Lactate reduces glutamate-induced neurotoxicity in rat cortex. J Neurosci Res 66:790-794.
24. Ruusuvuori E, Li H, Huttu K, Palva JM, Smirnov S, Rivera C, Kaila K, Voipio J (2004) Carbonic anhydrase isoform VII acts as a molecular switch in the development of synchronous gamma-frequency firing of hippocampal CA1 pyramidal cells. J Neurosci 24:2699-2707.
25. Sipilä 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 25:5280-5289.
26. Sipilä ST, Huttu K, Voipio J, Kaila K (2006a) Intrinsic bursting of immature CA3 pyramidal neurons and consequent giant depolarizing potentials are driven by a persistent Na+ current and terminated by a slow Ca2+- activated K+ current. Eur J Neurosci 23:2330-2338. (Pubitemid 43742865)
27. Sipilä ST, Schuchmann S, Voipio J, Yamada J, Kaila K (2006b) The cationchloride cotransporter NKCC1 promotes sharp waves in the neonatal rat hippocampus. J Physiol 573:765-773.
28. Tombaugh GC, Somjen GG (1998) pH modulation and voltage-gated ion channels. In: pH and brain function (Kaila K, Ransom BR, eds), pp 395-416. New York: Wiley.
29. Tyzio R, Allene C, Nardou R, Picardo MA, Yamamoto S, Sivakumaran S, Caiati MD, Rheims S, Minlebaev M, Ferré P, Khazipov R, Romette JL, Lorquin J, Cossart R, Khalilov I, Nehlig A, Cherubini E, Ben-Ari Y (2010) GABA action in immature cortical neurons neither depends on the availability of ketone bodies nor on pyruvate. J Neurosci, in press.
30. Willoughby D, Schwiening CJ (2002) Electrically evoked dendritic pH transients in rat cerebellar Purkinje cells. J Physiol 544:487-499.
31. 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)
32. York D (1966) Least-squares fitting of a straight line. Can J Phys 44:1079-1086.