Ion dynamics during seizures

Frontiers in Cellular Neuroscience

Volumn 9, Issue OCTOBER, 2015, Pages

  Raimondo, Joseph V ^a   Burman, Richard J ^a   Katz, Arieh A ^a   Akerman, Colin J ^b  

^a UNIVERSITY OF CAPE TOWN   (South Africa)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Calcium; Chloride; Epilepsy; Ion dynamics; pH; Potassium; Seizures; Sodium

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; ADENOSINE TRIPHOSPHATASE (CALCIUM); ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ANION; ANTICONVULSIVE AGENT; BENZODIAZEPINE; BICARBONATE; CALCIUM ION; CARBONATE DEHYDRATASE; CATION; CHLORIDE ION; GLUTAMIC ACID; HYDROGEN; NEUROTRANSMITTER; POTASSIUM CHLORIDE COTRANSPORTER 2; POTASSIUM ION; SODIUM CALCIUM EXCHANGE PROTEIN; SODIUM ION; SODIUM POTASSIUM CHLORIDE COTRANSPORTER 1; VALINOMYCIN;

BRAIN METABOLISM; DENDRITIC SPINE; EPILEPTIC DISCHARGE; EPILEPTIC FOCUS; EPILEPTIC STATE; GABAERGIC TRANSMISSION; GLUTAMATERGIC SYNAPSE; HUMAN; INTRACELLULAR SIGNALING; ION CURRENT; MEMBRANE DEPOLARIZATION; MEMBRANE POTENTIAL; MICROELECTRODE; MUTAGENESIS; NERVE CELL MEMBRANE; NERVE CELL MEMBRANE CONDUCTANCE; NERVOUS TISSUE; REVERSAL POTENTIAL; REVIEW; SEIZURE; SYNAPTIC TRANSMISSION; VISUAL CORTEX;

EID: 84947581801     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2015.00419     Document Type: Review

References (154)

1. Abad, M. F. C., Di Benedetto, G., Magalhaes, P. J., Filippin, L., and Pozzan, T. (2004). Mitochondrial pH monitored by a new engineered green fluorescent protein mutant. J. Biol. Chem 279, 11521-11529. doi: 10.1074/jbc.m306766200
2. Amzica, F., and Steriade, M. (2000). Neuronal and glial membrane potentials during sleep and paroxysmal oscillations in the neocortex. J. Neurosci. 20, 6648-6665.
3. Arosio, D., Ricci, F., Marchetti, L., Gualdani, R., Albertazzi, L., and Beltram ,(2010). Simultaneous intracellular chloride and pH measurements using a GFP-based sensor. Nat. Methods 7, 516-518. doi: 10.1038/nmeth.1471
4. Avoli, M., Louvel, J., Pumain, R., and Olivier, A. (1987). Seizure-like discharges induced by lowering [Mg2+]o in the human epileptogenic neocortex maintained in vitro. Brain Res. 417, 199-203.
5. Balestrino, M., and Somjen, G. G. (1988). Concentration of carbon dioxide, interstitial pH and synaptic transmission in hippocampal formation of the rat. J. Physiol. 396, 247-266. doi: 10.1113/jphysiol.1988.sp016961
6. Barnes, S., and Bui, Q. (1991). Modulation of calcium-activated chloride current via pH-induced changes of calcium channel properties in cone photoreceptors. J. Neurosci. 11,4015-4023.
7. Bedner, P., Dupper, A., Huttmann, K., Muller, J., Herde, M. K., Dublin, P., et al. (2015). Astrocyte uncoupling as a cause ofhuman temporallobe epilepsy. Brain 138, 1208-1222. doi: 10.1093/brain/awv067
8. Ben-Ari, Y. (2002). Excitatory actions of GABA during development: the nature of the nurture. Nat. Rev. Neurosci. 3, 728-739. doi: 10.1038/nrn920
9. Benninger, C., Kadis, J., and Prince, D. A. (1980). Extracellular calcium and potassium changes in hippocampal slices. Brain Res. 187, 165-182. doi: 10. 1016/0006-8993(80)90502-8
10. Berridge, M. J., Bootman, M. D., and Roderick, H. L. (2003). Calcium signalling: dynamics, homeostasis and remodelling. Nat. Rev. Mol. Cell Biol. 4, 517-529. doi: 10.1038/nrm1155
11. Bhattacharjee, A., Joiner, W. J., Wu, M., Yang, Y., Sigworth, F. J., and Kaczmarek, L. K. (2003). Slick (slo2.1), a rapidly-gating sodium-activated potassium channel inhibited byATP. J. Neurosci. 23, 11681-11691.
12. Bormann, J., Hamill, O. P., and Sakmann, B. (1987). Mechanism of anion permeation through channels gated by glycine and gamma-aminobutyric acid in mouse cultured spinal neurones. J. Physiol. 385, 243-286. doi: 10. 1113/jphysiol.1987.sp016493
13. Boyarsky, G., Ganz, M. B., Sterzel, R. B., and Boron, W. F. (1988). pH regulation in single glomerular mesangial cells. I. Acid extrusion in absence and presence ofHCO-. Am. J. Physiol. 255, C844-C856.
14. Bragin, A., Penttonen, M., and Buzsaki, G. (1997). Termination of epileptic afterdischarge in the hippocampus. J. Neurosci. 17, 2567-2579.
15. Buckler, K. J., andVaughan-Jones, R. D. (1990).Application of anewpH-sensitive fluoroprobe (carboxy-SNARF-1) for intracellular pH measurement in small, isolated cells. Pflugers Arch. 417, 234-239. doi: 10.1007/bf00370705
16. Butt, A. M., and Kalsi, A. (2006). Inwardly rectifying potassium channels (Kir) in central nervous system glia: A special role for Kir4.1 in glial functions. J. Cell. Mol. Med. 10, 33-44. doi: 10.1111/j.1582-4934.2006.tb00289.x
17. Caspers, H., and Speckmann, E. (1972). Cerebral pO2, pCO2 and pH: changes during convulsive activity and their significance for spontaneous arrest of seizures. Epilepsia 13, 699-725. doi: 10.1111/j.1528-1157.1972.tb04403.x
18. Chen, T. W., Wardill, T. J., Sun, Y., Pulver, S. R., Renninger, S. L., Baohan, A., et al. (2013). Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499, 295-300. doi: 10.1038/nature12354
19. Chesler, M. (2003). Regulation and modulation of pH in the brain. Physiol. Rev.83, 1183-1221. doi: 10.1152/physrev.00010.2003
20. Chesler, M., and Kraig, R. (1989). Intracellular pH transients of mammalian astrocytes. J. Neurosci. 9, 2011-2019.
21. Collingridge, G. L., and Bliss, T. V. P. (1987). NMDA receptors -their role in long-term potentiation. Trends Neurosci. 10, 288-293. doi: 10.1016/0166-2236(87)90175-5
22. Collins, F., Schmidt, M., Guthrie, P., and Kater, S. (1991). Sustained increase in intracellular calcium promotes neuronal survival. J. Neurosci. 11, 2582-2587
23. Danbolt, N. C. (2001). Glutamate uptake. Prog. Neurobiol 65, 1-105. doi: 10.1016/S0301-0082(00)00067-8 de
24. Curtis, M., and Manfridi, A. and Biella, G. (1998). Activity-dependent pH shifts and periodic recurrence of spontaneous interictal spikes in a model of focal epileptogenesis. J. Neurosci. 18, 7543-7551.
25. Deeb, T. Z., Nakamura, Y., Frost, G. D., and Davies, P. A. and Moss, S. J. (2013). Disrupted Cl(-) homeostasis contributes to reductions in the inhibitoryefficacy of diazepam duringhyperexcited states. Eur. J. Neurosci. 38,2453-2467. doi: 10. 1111/ejn.12241
26. Denker, S. P., and Barber, D. L. (2002). Cell migration requires both ion translocation and cytoskeletal anchoring by the Na-H exchanger NHE1. J. Cell Biol. 159, 1087-1096. doi: 10.1083/jcb.200208050
27. Diarra, A., Sheldon, C., and Church, J. (2001). In situ calibration and [H+] sensitivity of the fluorescent Na+ indicator SBFI. Am. J. Physiol. Cell Physiol. 280, C1623-C1633. doi: 10.1016/S0165-5876(00)00363-3
28. Dietzel, I., and Heinemann, U. (1986). Dynamic variations of the brain cell microenvironment in relation to neuronal hyperactivity. Ann. N Y Acad. Sci. 481,72-86. doi: 10.1111/j.1749-6632.1986.tb27140.x
29. Dietzel, I., Heinemann, U., Hofmeier, G., and Lux, H. D. (1982). Stimulus-induced Changes in Extracellular Na+ and Cl-Conc entration in Relation to Changes in the Size of the Extracellular Space. Exp. Brain Res. 46, 73-84. doi: 10. 1007/bf00238100
30. Doyon, N., Prescott, S. A., Castonguay, A., Godin, A. G., Kroger, H., and De Koninck, Y. (2011). Efficacy of synaptic inhibition depends on multiple, dynamically interacting mechanisms implicated in chloride homeostasis. PLoS Comput. Biol. 7:e1002149. doi: 10.1371/journal.pcbi.1002149
31. Drapeau, P., and Nachshen, D. A. (1988). Effects of lowering extracellular and cytosolic pH on calcium fluxes, cytosolic calcium levels and transmitter release in presynaptic nerve terminals isolated from rat. J. Gen. Physiol. 91, 305-315. doi: 10.1085/jgp.91.2.305
32. Dreier, J., and Heinemann, U. (1991). Regional and time dependent variations of lowMg2+ induced epileptiform activityin rat temporal cortex slices. Exp. Brain Res. 87, 581-596. doi: 10.1007/bf00227083
33. Dudek, F. E., Obenaus, A., and Tasker, J. G. (1990). Osmolality-induced changes in extracellular volume alter epileptiform bursts independent of chemical synapses in the rat: importance of non-synaptic mechanisms in hippocampal epileptogenesis. Neurosci. Lett. 120, 267-270. doi: 10.1016/0304-3940(90)90056-f
34. Dulla, C. G., Dobelis, P., Pearson, T., Frenguelli, B. G., Staley, K. J., and Masino, S. A. (2005). Adenosine and ATP link PCO2 to cortical excitability via pH. Neuron 48, 1011-1023. doi: 10.1016/j.neuron.2005.11.009
35. During, M. J., Ryder, K. M., and Spencer, D. D. (1995). Hippocampal GABA transporter function in temporal-lobe epilepsy. Nature 376, 174-177. doi: 10. 1038/376174a0
36. Ebert, U., Cramer, S., and Loscher, W. (1997). Phenytoin’s effect on the spread of seizure activity in the amygdala kindling model. Naunyn. Schmiedebergs. Arch. Pharmacol. 356, 341-347. doi: 10.1007/pl00005060
37. Egawa, K., Yamada, J., Furukawa, T., Yanagawa, Y., and Fukuda, A. (2013). Cl-homeodynamics in gap-junction-coupled astrocytic networks on activation of GABAergic synapses. J. Physiol. 591, 3901-3917. doi: 10.1113/jphysiol.2013. 257162
38. Ellender, T. J., Raimondo, J. V., Irkle, A., Lamsa, K. P., and Akerman, C. J. (2014). Excitatory effects of parvalbumin-expressing interneurons maintain hippocampal epileptiform activity via synchronous afterdischarges. J. Neurosci. 34, 15208-15222. doi: 10.1523/jneurosci.1747-14.2014
39. Fairman, W. A., Vandenberg, R. J., Arriza, J. L., Kavanaugh, M. P., and Amara, S. G. (1995). An excitatory amino-acid transporter with properties of a ligand-gated chloride channel. Nature 375, 599-603. doi: 10.1038/375599a0
40. Farrant, M., and Kaila, K. (2007). The cellular, molecular and ionic basis of GABAA receptor signalling. Prog. Brain Res. 160, 59-87. doi: 10.1016/s0079-6123(06)60005-8
41. Feng, Z., and Durand, D. M. (2003). Low-calcium epileptiform activity in the hippocampus in vivo. J. Neurophysiol. 90, 2253-2260. doi: 10.1152/jn.00241. 2003
42. Fertziger, A. P., and Ranck, J. B. (1970). Potassium accumulation in interstitial space during epileptiform seizures. Exp. Neurol. 26, 571-585. doi: 10. 1016/0014-4886(70)90150-0
43. Fleidervish, I. A., Lasser-Ross, N., Gutnick, M. J., and Ross, W. N. (2010). Na+ imaging reveals little difference in action potential-evoked Na+ influx between axon and soma. Nat. Neurosci. 13, 852-860. doi: 10.1038/nn.2574
44. Franklin, J. L., and Johnson, E. M. (1992). Suppression of programmed neuronal death by sustained elevation of cytoplasmic calcium. Trends Neurosci. 15, 501-508. doi: 10.1016/0166-2236(92)90103-f
45. Frohlich, F., Bazhenov, M., Iragui-Madoz, V., and Sejnowski, T. J. (2008). Potassium dynamics in the epileptic cortex: new insights on an old topic. Neuroscientist 14, 422-433. doi: 10.1177/1073858408317955
46. Frohlich, F., Bazhenov, M., Timofeev, I., Steriade, M., and Sejnowski, T. J. (2006). Slow state transitions of sustained neural oscillations by activity-dependent modulation of intrinsic excitability. J. Neurosci. 26, 6153-6162. doi: 10.1523/jneurosci.5509-05.2006
47. Frohlich, F., Sejnowski, T. J., and Bazhenov, M. (2010). Network bistability mediates spontaneous transitions between normal and pathological brain states. J. Neurosci. 30, 10734-10743. doi: 10.1523/jneurosci.1239-10.2010
48. Fujiwara-Tsukamoto, Y., Isomura, Y., Imanishi, M., Ninomiya, T., Tsukada, M., Yanagawa, Y., et al. (2010). Prototypic seizure activity driven by mature hippocampal fast-spiking interneurons. J. Neurosci. 30, 13679-13689. doi: 10. 1523/jneurosci.1523-10.2010
49. Gagnon, M., Bergeron, M. J., Lavertu, G., Castonguay, A., Tripathy, S., Bonin, R. P., et al. (2013). Chloride extrusion enhancers as novel therapeutics for neurological diseases. Nat. Med. 19, 1524-1528. doi: 10.1038/nm.3356
50. Ghosh, A., and Greenberg, M. E. (1995). Calcium signaling in neurons: molecular mechanisms and cellular consequences. Science 268, 239-247. doi: 10. 1126/science.7716515
51. Gnatkovsky, V., Librizzi, L., Trombin, F., and De Curtis, M. (2008). Fast activity at seizure onset is mediated by inhibitory circuits in the entorhinal cortex in vitro. Ann. Neurol. 64, 674-686. doi: 10.1002/ana.21519
52. Goldstein, S. A., Bockenhauer, D., O’Kelly, I., and Zilberberg, N. (2001). Potassium leak channels and the KCNK family of two-P-domain subunits. Nat. Rev. Neurosci. 2, 175-184. doi: 10.1038/35058574
53. Haas, H., and Jefferys, J. (1984). Low-calcium field burst discharges of CA1 pyramidal neurones in rat hippocampal slices. J. Physiol. 354, 185-201. doi: 10. 1113/jphysiol.1984.sp015371
54. Hinterkeuser, S., Schroder, W., Hager, G., Seifert, G., Blumcke, I., Elger, C. E., et al. (2000). Astrocytes in the hippocampus of patients with temporal lobe epilepsy display changes in potassium conductances. Eur. J. Neurosci. 12, 2087-2096. doi: 10.1046/j.1460-9568.2000.00104.x
55. Igelstrom, K. M. (2013). Is slack an intrinsic seizure terminator? Neuroscientist 19, 248-254. doi: 10.1177/1073858412446311
56. Iijima, T., Ciani, S., and Hagiwara, S. (1986). Effects of the external pH on Ca channels: experimental studies and theoretical considerations using a two-site, two-ion model. Proc. Natl. Acad. Sci. U S A 83, 654-658. doi: 10.1073/pnas.83. 3.654
57. Ilie, A., Raimondo, J. V., and Akerman, C. J. (2012). Adenosine release during seizures attenuates GABAA receptor-mediated depolarization. J. Neurosci. 32, 5321-5332. doi: 10.1523/jneurosci.5412-11.2012
58. Isomura, Y., Sugimoto, M., Fujiwara-Tsukamoto, Y., Yamamoto-Muraki, S., Yamada, J., and Fukuda, A. (2003). Synaptically activated Cl-accumulation responsible for depolarizing GABAergic responses in mature hippocampal neurons. J. Neurophysiol. 90,2752-2756. doi: 10.1152/jn.00142.2003
59. Jensen, M. S., Yaari, Y., Jiruska, P., Curtis, M. D., Jefferys, J. G. R., Schevon, C. A., et al. (2014). Role of intrinsic burst firing, potassium accumulation, and electrical coupling in the elevated potassium model of hippocampal epilepsy. J. Neurophysiol. 77, 1224-1233.
60. Jiang, C., and Haddad, G. G. (1991). Effect of anoxia on intracellular and extracellularpotassium activityin hypoglossal neurons in vitro. J. Neurophysiol. 66, 103-111.
61. Kaczmarek, L. K. (2013). Slack, slick and sodium-activated potassium channels. ISRNNeurosci. 2013, 1-14. doi: 10.1155/2013/354262
62. Kaila, K., and Voipio, J. (1987). Postsynaptic fall in intracellular pH induced by GABA-activated bicarbonate conductance. Nature 330, 163-165. doi: 10. 1038/330163a0
63. Kaila, K., Lamsa, K., Smirnov, S., Taira, T., and Voipio, J. (1997). Long-lasting GABA-mediated depolarization evoked by high-frequency stimulation in pyramidal neurons of rat hippocampal slice is attributable to a network-driven, bicarbonate-dependent K+ transient. J. Neurosci. 17, 7662-7672.
64. Kaila, K., Pasternack, M., Saarikoski, J., Voipio, J., and Britain, G. (1989). Influence of GABA-gated bicarbonate conductance on potential, current and intracellular chloride in crayfish muscle fibres. J. Physiol. 416, 161-181. doi: 10. 1113/jphysiol.1989.sp017755
65. Kaila, K., Price, T. J., Payne, J. A., Puskarjov, M., and Voipio, J. (2014a). Cation-chloride cotransporters in neuronal development, plasticity and disease. Nat. Rev. Neurosci. 15, 637-654. doi: 10.1038/nrn3819
66. Kaila, K., Ruusuvuori, E., Seja, P., Voipio, J., and Puskarjov, M. (2014b). GABA actions and ionic plasticity in epilepsy. Curr. Opin. Neurobiol. 26, 34-41. doi: 10.1016/j.conb.2013.11.004
67. Kaila, K., Saarikoski, J., and Voipio, J. (1990). Mechanism of action of GABA on intracellular pH and on surface pH in crayfish muscle fibres. J. Physiol. 427, 241-260. doi: 10.1113/jphysiol.1990.sp018170
68. Kaila, K., Voipio, J., Paalasmaa, P., Pasternack, M., and Deisz, R. (1993). The role ofbicarbonate in GABAA receptor-mediated IPSPs of rat neocortical neurones. J. Physiol. 464, 273-289. doi: 10.1113/jphysiol.1993.sp019634
69. Karus, C., Mondragao, M. A., Ziemens, D., and Rose, C. R. (2015). Astrocytes restrict discharge duration and neuronal sodium loads during recurrent network activity. Glia 63, 936-957. doi: 10.1002/glia.22793
70. Kneen, M., Farinas, J., Li, Y., and Verkman, A. S. (1998). Green fluorescentprotein as a noninvasive intracellular pH indicator. Biophys. J. 74, 1591-1599. doi: 10. 1016/s0006-3495(98)77870-1
71. Kofuji, P., and Newman, E. A. (2004). Potassium buffering in the central nervous system. Neuroscience 129, 1045-1056. doi: 10.1016/j.neuroscience.2004.06.008
72. Krishnan, G. P., and Bazhenov, M. (2011). Ionic dynamics mediate spontaneous termination of seizures and postictal depression state. J. Neurosci. 31, 8870-8882. doi: 10.1523/jneurosci.6200-10.2011
73. Krishnan, G. P., Filatov, G., Shilnikov, A., and Bazhenov, M. (2015). Electrogenic properties of the Na+/K+ ATPase control transitions between normal and pathological brain states. J. Neurophysiol. 113, 3356-3374. doi: 10.1152/jn. 00460.2014
74. Kuner, T., and Augustine, G. J. (2000). A genetically encoded ratiometric indicator for chloride: capturing chloride transients in cultured hippocampal neurons. Neuron 27, 447-459. doi: 10.1016/S0896-6273(00)00056-8
75. Kuramoto, T., and Haber, B. (1981). The K+ liquid ion exchange electrode system: responses to drugs and neurotransmitters. J. Neurosci. Res. 6, 37-48. doi: 10. 1002/jnr.490060105
76. Kyrozis, A., and Reichling, D. B. (1995). Perforated-patch recording with gramicidin avoids artifactual changes in intracellular chloride concentration. J. Neurosci. Methods. 57, 27-35. doi: 10.1016/0165-0270(94) 00116-x
77. Lamsa, K., and Kaila, K. (1997). Ionic mechanisms of spontaneous GABAergic events in rat hippocampal slices exposed to 4-aminopyridine. J. Neurophysiol. 78, 2582-2591.
78. Langer, J., and Rose, C. R. (2009). Synaptically induced sodium signals in hippocampal astrocytes in situ. J. Physiol. 587, 5859-5877. doi: 10.1113/jphysiol.2009.182279
79. Lesage, F. (2003). Pharmacology of neuronal background potassium channels. Neuropharmacology 44, 1-7. doi: 10.1016/s0028-3908(02)00339-8
80. Looger, L. L., and Griesbeck, O. (2012). Genetically encoded neural activity indicators. Curr. Opin. Neurobiol. 22, 18-23. doi: 10.1016/j.conb.2011.10.024
81. Makani, S., and Chesler, M. (2010). Rapid rise of extracellular pH evoked by neural activity is generated by the plasma membrane calcium ATPase. J. Neurophysiol. 103, 667-676. doi: 10.1152/jn.00948.2009
82. Markova, O., Mukhtarov, M., Real, E., Jacob, Y., and Bregestovski, P. (2008). Genetically encoded chloride indicator with improved sensitivity. J. Neurosci. Methods. 170, 67-76. doi: 10.1016/j.jneumeth.2007.12.016
83. McCormick, D. A., and Contreras, D. (2001). On the cellular and network bases of epileptic seizures. Annu. Rev. Physiol. 63, 815-846. doi: 10.1146/annurev.physiol.63.1.815
84. McDougal, D. B., and Osborn, L. A. (1976). Post-tetanic hyperpolarization, sodium-potassium-activated adenosine triphosphatase and high energy phosphate levels in garfish olfactory nerve. J. Physiol. 256, 41-60. doi: 10. 1113/jphysiol.1976.sp011310
85. McLaughlin, S. G., Szabo, G., and Eisenman, G. (1971). Divalent ions and the surface potential of charged phospholipid membranes. J. Gen. Physiol. 58, 667-687. doi: 10.1085/jgp.58.6.667
86. Meier, S. D., Kovalchuk, Y., and Rose, C. R. (2006). Properties of the new fluorescent Na+ indicator CoroNa Green: Comparison with SBFI and confocal Na+ imaging. J. Neurosci. Methods 155,251-259. doi: 10.1016/j.jneumeth.2006. 01.009
87. Minta, A., and Tsien, R. Y. (1989). Fluorescent indicators for cytosolic sodium. J. Biol. Chem. 264, 19449-19457.
88. Morth, J. P., Pedersen, B. P., Toustrup-Jensen, M. S., S0rensen, T. L. M., Petersen, J., Andersen, J. P., et al. (2007). Crystal structure of the sodium-potassium pump. Nature 450, 1043-1049. doi: 10.1038/nature06419
89. Neal, E. G., Chaffe, H., Schwartz, R. H., Lawson, M. S., Edwards, N., Fitzsimmons ,, et al. (2008). The ketogenic diet for the treatment of childhood epilepsy: a randomised controlled trial. Lancet Neurol. 7, 500-506. doi: 10.1016/S1474-4422(08)70092-9(08)70092-9
90. Olsson, T., Broberg, M., Pope, K. J., Wallace, A., Mackenzie, L., Blomstrand, F., et al. (2006). Cell swelling, seizures and spreading depression: animpedance study. Neuroscience140, 505-515. doi: 10.1016/j.neuroscience.2006. 02.034
91. Opie, L. (1965). Effect of extracellular pH on function and metabolism of isolated perfused rat heart. Am. J. Physiol. 209, 1075-1080.
92. Pal, S., Sombati, S., Limbrick, D. D., and DeLorenzo, R. J. (1999). In vitro status epilepticus causes sustained elevation of intracellular calcium levels in hippocampal neurons. Brain Res. 851, 20-31. doi: 10.1016/s0006-8993(99)02035-1
93. Pasternack, M., Smirnov, S., and Kaila, K. (1996). Proton modulation of functionally distinct gabaa receptors in acutely isolated pyramidal neurons of rat hippocampus. Neuropharmacology 35, 1279-1288. doi: 10.1016/s0028-3908(96)00075-5
94. Pasternack, M., Voipio, J., and Kaila, K. (1993). Intracellular carbonic anhydrase activity and its role in GABA-induced acidosis in isolated rat hippocampal pyramidal neurones. Acta. Physiol. Scand. 148, 229-231. doi: 10.1111/j.1748-1716.1993.tb09553.x
95. Pumain, R., Menini, C., and Heinemann, U. (1985). Chemical synaptic transmission is not necessary for epileptic seizures to persist in the baboon Papio papio. Exp. Neurol. 89, 250-258. doi: 10.1016/0014-4886(85)90280-8
96. Putney, L. K., and Barber, D. L. (2003). Na-H exchange-dependent increase in intracellular pH times G2/M entry and transition. J. Biol. Chem. 278, 44645-44649. doi: 10.1074/jbc.m308099200
97. Quednau, B. D., Nicoll, D. A., and Philipson, K. D. (2004). The sodium/calcium exchangerfamily-SLC8. Pflugers.Arch. 447, 543-548. doi: 10.1007/s00424-003-1065-4
98. Raimondo, J. V., Joyce, B., Kay, L., Schlagheck, T., Newey, S. E., Srinivas, S., et al. (2013). A genetically-encoded chloride and pH sensor for dissociatingion dynamics in the nervous system. Front. Cell. Neurosci. 7:202. doi: 10.3389/fncel. 2013.00202
99. Raimondo, J. V., Irkle, A., Wefelmeyer, W., Newey, S. E., and Akerman, C. J. (2012a). Genetically encoded proton sensors reveal activity-dependent pH changes in neurons. Front. Mol. Neurosci. 5:68. doi: 10.3389/fnmol.2012.00068
100. Raimondo, J. V., Markram, H., and Akerman, C. J. (2012b). Short-term ionic plasticity at GABAergic synapses. Front. Synaptic Neurosci. 4:5. doi: 10. 3389/fnsyn.2012.00005
101. Ransom, B. R., Carlini, W. G., and Yamate, C. L. (1987). Tip size of ion-exchanger based K+ -selective microelectrodes. II. Effects on measurement of evoked [K+] 0 transients. Can. J. Physiol. Pharmacol. 65, 894-897. doi: 10.1139/y87-144
102. Rimmele, T. S., and Chatton, J.-Y. (2014). A novel optical intracellular imaging approach for potassium dynamics in astrocytes. PLoS One 9:e109243. doi: 10. 1371/journal.pone.0109243
103. Ritchie, J. M., and Straub, R. W. (1957). The hyperpolarization which follows activity in mammalian non-medullated fibres. J. Physiol. 136, 80-97. doi: 10. 1113/jphysiol.1957.sp005744
104. Rivera, C., Voipio, J., and Kaila, K. (2005). Two developmental switches in GABAergic signalling: the K+-Cl-cotransporter KCC2 and carbonic anhydrase CAVII. J. Physiol. 562, 27-36. doi: 10.1113/jphysiol.2004.077495
105. Rivera, C., Voipio, J., Thomas-Crusells, J., Li, H., Emri, Z., Sipila, S., et al. (2004). Mechanism of activity-dependent downregulation of the neuron-specific K-Cl cotransporter KCC2. J. Neurosci. 24, 4683-4691. doi: 10.1523/jneurosci.5265-03.2004
106. Rose, C. R. (2003). High-resolution Na+ imaging in dendrites and spines. Pflugers Arch. 446, 317-321. doi: 10.1007/s00424-003-1036-9
107. Rose, C. R., and Deitmer, J. W. (1995). Stimulus-evoked changes of extra-and intracellular pH in the leech central nervous system. II. Mechanisms and maintenance of pH homeostasis. J. Neurophysiol. 73, 132-140.
108. Rose, C. R., and Konnerth, A. (2001). NMDA receptor-mediated Na+ signals in spines and dendrites. J. Neurosci. 21, 4207-4214.
109. Ruusuvuori, E., Li, H., Huttu, K., Palva, J. M., Smirnov, S., Rivera, C., et al. (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. doi: 10.1523/jneurosci.5176-03.2004
110. Schwiening, C. J., Kennedy, H. J., and Thomas, R. C. (1993). Calcium-hydrogen exchange by the plasma membrane Ca-ATPase of voltage-clamped snail neurons. Proc. R. Soc. Lond. B Biol. Sci. 253, 285-289. doi: 10.1098/rspb.1993. 0115
111. Singer, W., and Lux, H. D. (1975). Extracellular potassium gradients and visual receptive fields in the cat striate cortex. Brain Res. 96, 378-383. doi: 10. 1016/0006-8993(75)90751-9
112. Smart, T. G., and Constanti, A. (1982). A novel effect of zinc on the lobster muscle GABA receptor. Proc. R. Soc. Lond. B Biol. Sci. 215, 327-341. doi: 10.1098/rspb. 1982.0045
113. Somjen, G. G. (1980). Stimulus-evoked and seizure-related responses of extracellular calcium activity in spinal cord compared to those in cerebral cortex. J. Neurophysiol. 44, 617-632.
114. Sparing, R., Dafotakis, M., Buelte, D., Meister, I. G., and Noth, J. (2007). Excitability of human motor and visual cortex before, during and after hyperventilation. J. Appl. Physiol. 102, 406-411. doi: 10.1152/japplphysiol. 00770.2006
115. Spray, D., Harris, A., and Bennett, M. (1981). Gap junctional conductance is a simple and sensitive function of intracellular pH. Science 211, 712-715. doi: 10. 1126/science.6779379
116. Staley, K. J., and Proctor, W. R. (1999). Modulation of mammalian dendritic GABAA receptor function by the kinetics of Cl-and HCO3-transport. J. Physiol. 519, 693-712. doi: 10.1111/j.1469-7793.1999. 0693n.x
117. Staley, K. J., Soldo, B. L., and Proctor, W. R. (1995). Ionic mechanisms of neuronal excitation by inhibitory GABAA receptors. Science 269, 977-981. doi: 10. 1126/science.7638623
118. Steinhauser, C., and Seifert, G. (2002). Glial membrane channels and receptors in epilepsy: impact for generation and spread of seizure activity. Eur. J. Pharmacol. 447, 227-237. doi: 10.1016/s0014-2999(02)01846-0
119. Sykova, E., and Nicholson, C. (2008). Diffusion in brain extracellular space. Physiol. Rev. 88, 1277-1340. doi: 10.1152/physrev.00027.2007
120. Sypert, G. W., and Ward, A. A. (1974). Changes in extracellular potassium activity during neocortical propagated seizures. Exp. Neurol. 45, 19-41. doi: 10. 1016/0014-4886(74)90097-1
121. Tabb, J. S., Kish, P. E., Van Dyke, R., and Ueda, T. (1992). Glutamate transport into synaptic vesicles. Roles of membrane potential, pH gradient and intravesicular pH. J. Biol. Chem. 267, 15412-15418.
122. Takeuchi, A., and Takeuchi, N. (1967). Anion permeability of the inhibitory post-synaptic membrane of the crayfish neuromuscular junction. J. Physiol. 191, 575-590 doi: 10.1113/jphysiol.1967.sp008269
123. Tang, C. M., Dichter, M., and Morad, M. (1990). Modulation of the N-Methyl-D-Aspartate Channel by Extracellular H+. Proc. Natl. Acad. Sci. USA 87, 6445-6449. doi: 10.1073/pnas.87.16.6445
124. Taylor, C. P., and Dudek, F. E. (1982). Synchronous neural afterdischarges in rat hippocampal slices without active chemical synapses. Science 218, 810-812. doi: 10.1126/science.7134978
125. Thompson, S. M., and Gahwiler, B. H. (1989). Activity-dependent disinhibition. I. Repetitive stimulation reduces IPSP driving force and conductance in the hippocampus in vitro. J. Neurophysiol. 61, 501-511.
126. Thompson, S. M., and Prince, D. A. (1986). Activation of electrogenic sodium pump in hippocampal CA1 neurons following glutamate-induced depolarization. J. Neurophysiol. 56, 507-522.
127. Tolner, E. A., Hochman, D. W., Hassinen, P., Otahal, J., Gaily, E., Haglund, M. M., et al. (2011). Five percent CO2 is a potent, fast-acting inhalation anticonvulsant. Epilepsia 52, 104-114. doi: 10.1111/j.1528-1167.2010.02731.x
128. Tombaugh, G. C. (1998). Intracellular pH Buffering Shapes Activity-Dependent Ca2+ Dynamics in Dendrites of CA1 Interneurons. J. Neurophysiol. 80, 1702-1712.
129. Tombaugh, G. C., and Somjen, G. G. (1997). DifferentialSensitivityto Intracellular pH Among High-and Low-Threshold Ca2+ Currents in Isolated Rat CA1 Neurons. J. Neurophysiol. 77, 639-653.
130. Trapp, S., Luckermann, M., Brooks, P. A., and Ballanyi, K. (1996). Acidosis of rat dorsal vagal neurons in situ during spontaneous and evoked activity. J. Physiol. 496, 695-710. doi: 10.1113/jphysiol.1996.sp021720
131. Traynelis, S. F., and Cull-Candy, S. G. (1990). Proton inhibition of N-methyl-D-aspartate receptors in cerebellar neurons. Nature 345, 347-350. doi: 10. 1038/345347a0
132. Traynelis, S. F., and Dingledine, R. (1988). Potassium-induced spontaneous electrographic seizures in the rat hippocampal slice. J. Neurophysiol. 59, 259-276.
133. Trevelyan, A. J., Sussillo, D., and Yuste, R. (2007). Feedforward inhibition contributes to the control of epileptiform propagation speed. J. Neurosci. 27, 3383-3387. doi: 10.1523/jneurosci.0145-07.2007
134. Tyzio, R., Minlebaev, M., Rheims, S., Ivanov, A., Jorquera, I., Holmes, G. L., et al. (2008). Postnatal changes in somatic gamma-aminobutyric acid signalling inthe rat hippocampus. Eur. J. Neurosci. 27,2515-2528. doi: 10.1111/j.1460-9568. 2008.06234.x
135. Urbanics, R., Leniger-Follert, E., and Lubbers, D. W. (1978). Time course of changes of extracellular H+ and K+ activities during and after direct electrical stimulation of the brain cortex. Pflugers Arch. 378,47-53.
136. Velisek, L., and Veliskova, J. (1993). Anticonvulsant action of carbonic anhydrase inhibition. Sb. Lek. 95, 161-171.
137. Vergara, C. (1998). Calcium-activated potassium channels. Curr. Opin. Neurobiol. 8, 321-329.
138. Viitanen, T., Ruusuvuori, E., Kaila, K., and Voipio, J. (2010). The K+-Cl cotransporter KCC2 promotes GABAergic excitation in the mature rat hippocampus. J. Physiol. 588, 1527-1540. doi: 10.1113/jphysiol.2009.181826
139. Volterra, A., Liaudet, N., and Savtchouk, I. (2014). Astrocyte Ca(2+) signalling: an unexpected complexity. Nat. Rev. Neurosci. 15, 327-335. doi: 10.1038/nrn3725
140. Vyklicky, L., Vlachova, V., and Krusek, J. (1990). The effect of external pH changes on responses to excitatory amino acids in mouse hippocampal neurones. J. Physiol. 430,497-517. doi: 10.1113/jphysiol.1990.sp018304
141. Walker, J. L. (1971). Ion Specific Liquid Ion Exchanger Microelectrodes. Anal.Chem. 43, 89A-93A. doi: 10.1021/ac60298a039
142. Wallraff, A., Kohling, R., Heinemann, U., Theis, M., Willecke, K., and Steinhauser, C. (2006). The impact of astrocytic gap junctional coupling on potassium buffering in the hippocampus. J. Neurosci. 26, 5438-5447. doi: 10. 1523/jneurosci.0037-06.2006
143. Walz, W. (2000). Role of astrocytes in the clearance of excess extracellular potassium. Neurochem. Int. 36, 291-300. doi: 10.1016/s0197-0186(99)00137-0
144. Wang, G. J., Randall, R. D., and Thayer, S. A. (1994). Glutamate-induced intracellular acidification of cultured hippocampal neurons demonstrates altered energy metabolism resulting from Ca2+ loads. J. Neurophysiol. 72, 2563-2569.
145. West, M. J., and Gundersen, H. J. (1990). Unbiased stereological estimation of the number of neurons in the human hippocampus. J. Comp. Neurol. 296, 1-22. doi: 10.1002/cne.902960102
146. Wood, J. N. (2001). Voltage-gated sodium channels. Curr. Opin. Pharmacol. 1, 17-21. doi: 10.1016/S1471-4892(01)00007-8
147. Wu, Y., Wang, W., Dickez-Sampedro, A., and Richerson, G. B. (2007). Nonvesicular inhibitory neurotransmission via reversal of the GABA transporter GAT-1. Neuron 56, 851-865. doi: 10.1016/j.neuron.2007.10.021
148. Xiong, Z. Q., and Stringer, J. L. (2000). Regulation of extracellular pH in the developing hippocampus. Brain Res. Dev. Brain Res. 122, 113-117. doi: 10. 1016/s0165-3806(00)00057-2
149. Xiong, Z. Q., Saggau, P., and Stringer, J. L. (2000). Activity-dependent intracellular acidification correlates with the duration of seizure activity. J. Neurosci. 20, 1290-1296.
150. Yaari, Y., Konnerth, A., and Heinemann, U. (1986). Nonsynaptic epileptogenesis in the mammalian hippocampus in vitro. II. Role of extracellular potassium. J. Neurophysiol. 56, 424-438.
151. Yang, Z., and Jiang, C. (1999). Opposite effects of pH on open-state probability and single channel conductance of kir4.1 channels. J. Physiol. 520, 921-927. doi: 10.1111/j.1469-7793.1999.00921.x
152. Yasiry, Z., and Shorvon, S. D. (2014). The relative effectiveness offive antiepileptic drugs in treatment of benzodiazepine-resistant convulsive status epilepticus: a meta-analysis of published studies. Seizure 23, 167-174. doi: 10.1016/j.seizure. 2013.12.007
153. Yellen, G. (2002). The voltage-gated potassium channels and their relatives. Nature 419, 35-42. doi: 10.1038/nature00978
154. Yuan, A., Santi, C. M., Wei, A., Wang, Z. W., Pollak, K., Nonet, M., et al. (2003). The sodium-activated potassium channel is encoded by a member of the Slo gene family. Neuron 37, 765-773. doi: 10.3410/f.1012796.187202