Extracellular potassium regulates the chloride reversal potential in cultured hippocampal neurons

Brain Research

Volumn 1205, Issue , 2008, Pages 12-20

  Balena, Trevor ^a   Acton, Brooke A ^a   Koval, Dmitrii ^a   Woodin, Melanie A ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

Chloride; Extracellular potassium; GABA; Hippocampus; Inhibitory synaptic transmission; KCC2

Indexed keywords

CHLORIDE; POTASSIUM; POTASSIUM CHLORIDE; POTASSIUM CHLORIDE COTRANSPORTER; SODIUM POTASSIUM CHLORIDE COTRANSPORTER; TETRODOTOXIN; TUBULIN;

ACTION POTENTIAL; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DEPOLARIZATION; EMBRYO; GABAERGIC SYSTEM; GABAERGIC TRANSMISSION; HIPPOCAMPUS; HYPERPOLARIZATION; MEMBRANE STEADY POTENTIAL; NONHUMAN; PATCH CLAMP; PERFUSION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REGULATORY MECHANISM; WESTERN BLOTTING;

ACTION POTENTIALS; ALGORITHMS; ANIMALS; BLOTTING, WESTERN; CELLS, CULTURED; CHLORIDES; ELECTROPHYSIOLOGY; FEMALE; GAMMA-AMINOBUTYRIC ACID; HIPPOCAMPUS; MEMBRANE POTENTIALS; NEURONS; PATCH-CLAMP TECHNIQUES; POTASSIUM; PREGNANCY; RATS; SODIUM-POTASSIUM-CHLORIDE SYMPORTERS; SYMPORTERS; SYNAPTIC TRANSMISSION;

MAMMALIA;

EID: 41949133231     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2008.02.038     Document Type: Article

References (42)

1. Akerman C.J., and Cline H.T. Depolarizing GABAergic conductances regulate the balance of excitation to inhibition in the developing retinotectal circuit in vivo. J. Neurosci. 26 (2006) 5117-5130
2. Ben-Ari Y. Excitatory actions of gaba during development: the nature of the nurture. Nat. Rev., Neurosci. 3 (2002) 728-739
3. Bi G.Q., and Poo M.M. Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type. J. Neurosci. 18 (1998) 10464-10472
4. Cancedda L., Fiumelli H., Chen K., and Poo M.M. Excitatory GABA action is essential for morphological maturation of cortical neurons in vivo. J. Neurosci. 27 (2007) 5224-5235
5. Delpire E. Cation-chloride cotransporters in neuronal communication. News Physiol. Sci. 15 (2000) 309-312
6. Dzhala V.I., Talos D.M., Sdrulla D.A., Brumback A.C., Mathews G.C., Benke T.A., Delpire E., Jensen F.E., and Staley K.J. NKCC1 transporter facilitates seizures in the developing brain. Nat. Med. 11 (2005) 1205-1213
7. Fiumelli H., and Woodin M.A. Role of activity-dependent regulation of neuronal chloride homeostasis in development. Curr. Opin. Neurobiol. 17 (2007) 81-86
8. Ganguly K., Schinder A.F., Wong S.T., and Poo M. GABA itself promotes the developmental switch of neuronal GABAergic responses from excitation to inhibition. Cell 105 (2001) 521-532
9. Gulledge A.T., and Stuart G.J. Excitatory actions of GABA in the cortex. Neuron 37 (2003) 299-309
10. Hablitz J.J., and Heinemann U. Alterations in the microenvironment during spreading depression associated with epileptiform activity in the immature neocortex. Brain Res. Dev. Brain Res. 46 (1989) 243-252
11. Jarolimek W., Lewen A., and Misgeld U. A furosemide-sensitive K+-Cl- cotransporter counteracts intracellular Cl- accumulation and depletion in cultured rat midbrain neurons. J. Neurosci. 19 (1999) 4695-4704
12. Kaila K. Ionic basis of GABAA receptor channel function in the nervous system. Prog. Neurobiol. 42 (1994) 489-537
13. Kaila K., and Voipio J. Postsynaptic fall in intracellular pH induced by GABA-activated bicarbonate conductance. Nature 330 (1987) 163-165
14. Kaila K., Voipio J., Paalasmaa P., Pasternack M., and Deisz R.A. The role of bicarbonate in GABAA receptor-mediated IPSPs of rat neocortical neurones. J. Physiol. 464 (1993) 273-289
15. Khirug S., Huttu K., Ludwig A., Smirnov S., Voipio J., Rivera C., Kaila K., and Khiroug L. Distinct properties of functional KCC2 expression in immature mouse hippocampal neurons in culture and in acute slices. Eur. J. Neurosci. 21 (2005) 899-904
16. Korn S.J., Giacchino J.L., Chamberlin N.L., and Dingledine R. Epileptiform burst activity induced by potassium in the hippocampus and its regulation by GABA-mediated inhibition. J. Neurophysiol. 57 (1987) 325-340
17. Lasher R.S., and Zagon I.S. The effect of potassium on neuronal differentiation in cultures of dissociated newborn rat cerebellum. Brain Res. 41 (1972) 482-488
18. Leitch E., Coaker J., Young C., Mehta V., and Sernagor E. GABA type-A activity controls its own developmental polarity switch in the maturing retina. J. Neurosci. 25 (2005) 4801-4805
19. Ludwig A., Li H., Saarma M., Kaila K., and Rivera C. Developmental up-regulation of KCC2 in the absence of GABAergic and glutamatergic transmission. Eur. J. Neurosci. 18 (2003) 3199-3206
20. Mattson M.P., and Kater S.B. Development and selective neurodegeneration in cell cultures from different hippocampal regions. Brain Res. 490 (1989) 110-125
21. McBain C.J. Hippocampal inhibitory neuron activity in the elevated potassium model of epilepsy. J. Neurophysiol. 73 (1995) 2853-2863
22. Mercado A., Mount D.B., and Gamba G. Electroneutral cation-chloride cotransporters in the central nervous system. Neurochem. Res. 29 (2004) 17-25
23. Nakanishi K., Yamada J., Takayama C., Oohira A., and Fukuda A. NKCC1 activity modulates formation of functional inhibitory synapses in cultured neocortical neurons. Synapse 61 (2007) 138-149
24. Payne J.A. Functional characterization of the neuronal-specific K-Cl cotransporter: implications for [K+]o regulation. Am. J. Physiol. 273 (1997) C1516-C1525
25. Payne J.A., Rivera C., Voipio J., and Kaila K. Cation-chloride co-transporters in neuronal communication, development and trauma. Trends Neurosci. 26 (2003) 199-206
26. Purves D., Augustine G.J., Fitzpatrick D., Hall W.C., LaMantia A.-S., McNamara J.O., and White L.E. Neuroscience. Fourth Edition (2008), Sinauer, Sunderland, MA
27. Rausche G., Igelmund P., and Heinemann U. Effects of changes in extracellular potassium, magnesium and calcium concentration on synaptic transmission in area CA1 and the dentate gyrus of rat hippocampal slices. Pflugers Arch. 415 (1990) 588-593
28. Rivera C., Voipio J., and Kaila K. Two developmental switches in GABAergic signalling: the K+-Cl- cotransporter KCC2 and carbonic anhydrase CAVII. J. Physiol. 562 (2005) 27-36
29. Rivera C., Voipio J., Payne J.A., Ruusuvuori E., Lahtinen H., Lamsa K., Pirvola U., Saarma M., and Kaila K. The K+/Cl- co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 397 (1999) 251-255
30. Ruusuvuori E., Li H., Huttu K., Palva J.M., Smirnov S., Rivera C., Kaila K., and Voipio J. 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 (2004) 2699-2707
31. Shin D.S., Ghai H., Cain S.W., and Buck L.T. Gap junctions do not underlie changes in whole-cell conductance in anoxic turtle brain. Comp. Biochem. Physiol., Part A Mol. Integr. Physiol. 134 (2003) 181-194
32. Somjen G.G. Extracellular potassium in the mammalian central nervous system. Annu. Rev. Physiol. 41 (1979) 159-177
33. Somjen G.G. Ion regulation in the brain: implications for pathophysiology. Neurosci. 8 (2002) 254-267
34. Somjen G.G., Dingledine R., Conners B., and Allen B. Extracellular potassium and calcium activities in the mammalian spinal cord, and the effect of changing ion levels on mammalian neural tissues. In: Sykova E., Hnik P., and Vyklicky L. (Eds). Ion-Selective Microelectrodes and Their Use in Excitable Tissues (1981), Plenum Press, New York 159-180
35. Spruston N., and Johnston D. Perforated patch-clamp analysis of the passive membrane properties of three classes of hippocampal neurons. J. Neurophysiol. 67 (1992) 508-529
36. Thompson S.M., and Gahwiler B.H. Activity-dependent disinhibition. II. Effects of extracellular potassium, furosemide, and membrane potential on ECl- in hippocampal CA3 neurons. J. Neurophysiol. 61 (1989) 512-523
37. Titz S., Hans M., Kelsch W., Lewen A., Swandulla D., and Misgeld U. Hyperpolarizing inhibition develops without trophic support by GABA in cultured rat midbrain neurons. J. Physiol. 550 (2003) 719-730
38. Verheugen J.A., Fricker D., and Miles R. Noninvasive measurements of the membrane potential and GABAergic action in hippocampal interneurons. J. Neurosci. 19 (1999) 2546-2555
39. Wilcox K.S., Buchhalter J., and Dichter M.A. Properties of inhibitory and excitatory synapses between hippocampal neurons in very low density cultures. Synapse 18 (1994) 128-151
40. Wojcik S.M., Katsurabayashi S., Guillemin I., Friauf E., Rosenmund C., Brose N., and Rhee J.S. A shared vesicular carrier allows synaptic corelease of GABA and glycine. Neuron 50 (2006) 575-587
41. Woodin M.A., Ganguly K., and Poo M.M. Coincident pre- and postsynaptic activity modifies GABAergic synapses by postsynaptic changes in Cl- transporter activity. Neuron 39 (2003) 807-820
42. Yamada J., Okabe A., Toyoda H., Kilb W., Luhmann H.J., and Fukuda A. Cl- uptake promoting depolarizing GABA actions in immature rat neocortical neurones is mediated by NKCC1. J. Physiol. 557 (2004) 829-841