How do astrocytes shape synaptic transmission? Insights from electrophysiology

Frontiers in Cellular Neuroscience

Volumn , Issue OCT, 2013, Pages

  Dallérac, Glenn ^a   Chever, Oana ^a   Rouach, Nathalie ^a  

^a Centre de Recherche Interdisciplinaire en Biologie   (France)

Author keywords

Dual recordings; Electrophysiology; Glia; Ionic channels; Neuroglial interactions; Neurons; Plasticity; Synapses

Indexed keywords

CALCIUM CHANNEL; CALCIUM ION; CHLORIDE CHANNEL; GLUTAMATE TRANSPORTER; POTASSIUM CHANNEL; SODIUM CHANNEL; SODIUM ION;

ASTROCYTE; BRAIN ELECTROPHYSIOLOGY; CALCIUM SIGNALING; CELL ACTIVATION; CELL FUNCTION; CELL INTERACTION; CELL MEMBRANE CONDUCTANCE; CELL MEMBRANE POTENTIAL; ENERGY METABOLISM; GAP JUNCTION; HUMAN; HYPERPOLARIZATION; ION CURRENT; MACROGLIA; MONITORING; NERVE CELL; NERVE CELL PLASTICITY; NONHUMAN; PROTEIN EXPRESSION; REVIEW; SYNAPSE; SYNAPTIC TRANSMISSION;

EID: 84886843302     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2013.00159     Document Type: Review

References (202)

1. Adermark, L., and Lovinger, D. M. (2008). Electrophysiological properties and gap junction coupling of striatal astrocytes. Neurochem. Int. 52, 1365-1372. doi: 10.1016/j.neuint.2008.02.006
2. Agulhon, C., Fiacco, T. A., and McCarthy, K. D. (2010). Hippocampal short-and long-term plasticity are not modulated by astrocyte Ca2+ signaling. Science 327, 1250-1254. doi: 10.1126/science.1184821
3. Aitken, P. G., and Somjen, G. G. (1986). The sources of extracellular potassium accumulation in the CA1 region of hippocampal slices. Brain Res. 369, 163-167. doi: 10.1016/0006-8993(86)90524-X
4. Amato, A., Barbour, B., Szatkowski, M., and Attwell, D. (1994). Counter-transport of potassium by the glutamate uptake carrier in glial cells isolated from the tiger salamander retina. J. Physiol. 479, 371-380.
5. Amedee, T., Robert, A., and Coles, J. A. (1997). Potassium homeostasis and glial energy metabolism. Glia 21, 46-55. doi: 10.1002/(SICI)1098-1136(199709)21:1<46::AID-GLIA5>3.0.CO;2-#
6. Amzica, F. (2002). In vivo electrophysiological evidences for cortical neuron-glia interactions during slow (<1 Hz) and paroxysmal sleep oscillations. J. Physiol. Paris96, 209-219. doi: 10.1016/S0928-4257(02)00008-6
7. Amzica, F., and Massimini, M. (2002). Glial and neuronal interactions during slow wave and paroxysmal activities in the neocortex. Cereb. Cortex 12, 1101-1113. doi: 10.1093/cercor/12.10.1101
8. Amzica, F., Massimini, M., and Manfridi, A. (2002). Spatial buffering during slow and paroxysmal sleep oscillations in cortical networks of glial cells in vivo. J. Neurosci. 22, 1042-1053.
9. Amzica, F., and Neckelmann, D. (1999). Membrane capacitance of cortical neurons and glia during sleep oscillations and spike-wave seizures. J. Neurophysiol. 82, 2731-2746.
10. Anderson, C. M., and Swanson, R. A. (2000). Astrocyte glutamate transport: review of properties, regulation, and physiological functions. Glia 32, 1-14. doi: 10.1002/1098-1136(200010)32:1<1::AID-GLIA10>3.3.CO;2-N
11. Angulo, M. C., Kozlov, A. S., Charpak, S., and Audinat, E. (2004). Glutamate released from glial cells synchronizes neuronal activity in the hippocampus. J. Neurosci. 24, 6920-6927. doi: 10.1523/JNEUROSCI.0473-04.2004
12. Araque, A., Martín, E. D., Perea, G., Arellano, J. I., and Buño, W. (2002). Synaptically released acetylcholine evokes Ca2+ elevations in astrocytes in hippocampal slices. J. Neurosci. 22, 2443-2450.
13. Araque, A., Parpura, V., Sanzgiri, R. P., and Haydon, P. G. (1998a). Glutamate-dependent astrocyte modulation of synaptic transmission between cultured hippocampal neurons. Eur. J. Neurosci. 10, 2129-2142. doi: 10.1046/j.1460-9568.1998.00221.x
14. Araque, A., Sanzgiri, R. P., Parpura, V., and Haydon, P. G. (1998b). Calcium elevation in astrocytes causes an NMDA receptor-dependent increase in the frequency of miniature synaptic currents in cultured hippocampal neurons. J. Neurosci. 18, 6822-6829.
15. Ballanyi, K., Grafe, P., and ten Bruggencate, G. (1987). Ion activities and potassium uptake mechanisms of glial cells in guinea-pig olfactory cortex slices. J. Physiol. 382, 159-174.
16. Barbour, B., Brew, H., and Attwell, D. (1988). Electrogenic glutamate uptake in glial cells is activated by intracellular potassium. Nature 335, 433-435. doi: 10.1038/335433a0
17. Barbour, B., Brew, H., and Attwell, D. (1991). Electrogenic uptake of glutamate and aspartate into glial cells isolated from the salamander (Ambystoma) retina. J. Physiol. 436, 169-193.
18. Barres, B. A. (1991). Glial ion channels. Curr. Opin. Neurobiol. 1, 354-359. doi: 10.1016/0959-4388(91)90052-9
19. Bay, V., and Butt, A. M. (2012). Relationship between glial potassium regulation and axon excitability: a role for glial Kir4.1 channels. Glia 60, 651-660. doi: 10.1002/glia.22299
20. Bellamy, T. C., and Ogden, D. (2005). Short-term plasticity of Bergmann glial cell extrasynaptic currents during parallel fiber stimulation in rat cerebellum. Glia 52, 325-335. doi: 10.1002/glia.20248
21. Bellamy, T. C., and Ogden, D. (2006). Long-term depression of neuron to glial signalling in rat cerebellar cortex. Eur. J. Neurosci. 23, 581-586. doi: 10.1111/j.1460-9568.2005.04588.x
22. Ben Achour, S., and Pascual, O. (2012). Astrocyte-neuron communication: functional consequences. Neurochem. Res. 37, 2464-2473. doi: 10.1007/s11064-012-0807-0
23. Benedetti, B., Matyash, V., and Kettenmann, H. (2011). Astrocytes control GABAergic inhibition of neurons in the mouse barrel cortex. J. Physiol. 589, 1159-1172. doi: 10.1113/jphysiol.2010.203224
24. Benediktsson, A. M., Marrs, G. S., Tu, J. C., Worley, P. F., Rothstein, J. D., Bergles, D. E., et al. (2012). Neuronal activity regulates glutamate transporter dynamics in developing astrocytes. Glia 60, 175-188. doi: 10.1002/glia.21249
25. Bennay, M., Langer, J., Meier, S. D., Kafitz, K. W., and Rose, C. R. (2008). Sodium signals in cerebellar Purkinje neurons and Bergmann glial cells evoked by glutamatergic synaptic transmission. Glia 56, 1138-1149. doi: 10.1002/glia.20685
26. Bergles, D. E., Jabs, R., and Steinhauser, C. (2010). Neuron-glia synapses in the brain. Brain Res. Rev. 63, 130-137. doi: 10.1016/j.brainresrev.2009.12.003
27. Bergles, D. E., and Jahr, C. E. (1997). Synaptic activation of glutamate transporters in hippocampal astrocytes. Neuron 19, 1297-1308. doi: 10.1016/S0896-6273(00)80420-1
28. Bernardinelli, Y., and Chatton, J.-Y. (2008). Differential effects of glutamate transporter inhibitors on the global electrophysiological response of astrocytes to neuronal stimulation. Brain Res. 1240, 47-53. doi: 10.1016/j.brainres.2008.09.014
29. Bernardinelli, Y., Magistretti, P. J., and Chatton, J.-Y. (2004). Astrocytes generate Na+-mediated metabolic waves. Proc. Natl. Acad. Sci. U.S.A. 101, 14937-14942. doi: 10.1073/pnas.0405315101
30. Bordey, A., Lyons, S. A., Hablitz, J. J., and Sontheimer, H. (2001). Electrophysiological characteristics of reactive astrocytes in experimental cortical dysplasia. J. Neurophysiol. 85, 1719-1731.
31. Bordey, A., and Sontheimer, H. (1997). Postnatal development of ionic currents in rat hippocampal astrocytes in situ. J. Neurophysiol. 78, 461-477.
32. Bordey, A., and Sontheimer, H. (1998). Electrophysiological properties of human astrocytic tumor cells in situ: enigma of spiking glial cells. J. Neurophysiol. 79, 2782-2793.
33. Brew, H., and Attwell, D. (1987). Electrogenic glutamate uptake is a major current carrier in the membrane of axolotl retinal glial cells. Nature 327, 707-709. doi: 10.1038/327707a0
34. Brockhaus, J., and Deitmer, J. W. (2002). Long-lasting modulation of synaptic input to Purkinje neurons by Bergmann glia stimulation in rat brain slices. J. Physiol. 545, 581-593. doi: 10.1113/jphysiol.2002.028423
35. 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
36. Castellucci, V. F., and Goldring, S. (1970). Contribution to steady potential shifts of slow depolarization in cells presumed to be glia. Electroencephalogr. Clin. Neurophysiol. 28, 109-118. doi: 10.1016/0013-4694(70)90178-1
37. Chatton, J. Y., Marquet, P., and Magistretti, P. J. (2000). A quantitative analysis of L-glutamate-regulated Na+ dynamics in mouse cortical astrocytes: implications for cellular bioenergetics. Eur. J. Neurosci. 12, 3843-3853. doi: 10.1046/j.1460-9568.2000.00269.x
38. Chatton, J.-Y., Pellerin, L., and Magistretti, P. J. (2003). GABA uptake into astrocytes is not associated with significant metabolic cost: implications for brain imaging of inhibitory transmission. Proc. Natl. Acad. Sci. U.S.A. 100, 12456-12461. doi: 10.1073/pnas.2132096100
39. Chaudhry, F. A., Lehre, K. P., Lookeren Campagne, M., van, Ottersen, O. P., Danbolt, N. C., and Storm-Mathisen, J. (1995). Glutamate transporters in glial plasma membranes: highly differentiated localizations revealed by quantitative ultrastructural immunocytochemistry. Neuron 15, 711-720. doi: 10.1016/0896-6273(95)90158-2
40. Chen, N., Sugihara, H., Sharma, J., Perea, G., Petravicz, J., and Le, C. (2012). Nucleus basalis-enabled stimulus-specific plasticity in the visual cortex is mediated by astrocytes. Proc. Natl. Acad. Sci. U.S.A. 109, E2832-E2841. doi: 10.1073/pnas.1206557109
41. Chesler, M., and Kraig, R. P. (1987). Intracellular pH of astrocytes increases rapidly with cortical stimulation. Am. J. Physiol. 253, R666-R670.
42. Chesler, M., and Kraig, R. P. (1989). Intracellular pH transients of mammalian astrocytes. J. Neurosci. 9, 2011-2019.
43. Chever, O., Djukic, B., McCarthy, K. D., and Amzica, F. (2010). Implication of Kir4.1 channel in excess potassium clearance: an in vivo study on anesthetized glial-conditional Kir4.1 knock-out mice. J. Neurosci. 30, 15769-15777. doi: 10.1523/JNEUROSCI.2078-10.2010
44. Chvátal, A., Pastor, A., Mauch, M., Syková, E., and Kettenmann, H. (1995). Distinct populations of identified glial cells in the developing rat spinal cord slice: ion channel properties and cell morphology. Eur. J. Neurosci. 7, 129-142. doi: 10.1111/j.1460-9568.1995.tb01027.x
45. Clark, B. A., and Barbour, B. (1997). Currents evoked in Bergmann glial cells by parallel fibre stimulation in rat cerebellar slices. J. Physiol. 502, 335-350. doi: 10.1111/j.1469-7793.1997.335bk.x
46. Connors, B. W., Ransom, B. R., Kunis, D. M., and Gutnick, M. J. (1982). Activity-dependent K+ accumulation in the developing rat optic nerve. Science 216, 1341-1343. doi: 10.1126/science.7079771
47. Cornell-Bell, A. H., Finkbeiner, S. M., Cooper, M. S., and Smith, S. J. (1990). Glutamate induces calcium waves in cultured astrocytes: long-range glial signaling. Science 247, 470-473. doi: 10.1126/science.1967852
48. D'Ambrosio, R., Gordon, D. S., and Winn, H. R. (2002). Differential role of KIR channel and Na(+)/K(+)-pump in the regulation of extracellular K(+) in rat hippocampus. J. Neurophysiol. 87, 87-102.
49. Danbolt, N. C. (2001). Glutamate uptake. Prog. Neurobiol. 65, 1-105. doi: 10.1016/S0301-0082(00)00067-8
50. Dani, J. W., Chernjavsky, A., and Smith, S. J. (1992). Neuronal activity triggers calcium waves in hippocampal astrocyte networks. Neuron 8, 429-440. doi: 10.1016/0896-6273(92)90271-E
51. Davie, J. T., Kole, M. H. P., Letzkus, J. J., Rancz, E. A., Spruston, N., Stuart, G. J., et al. (2006). Dendritic patch-clamp recording. Nat. Protoc. 1, 1235-1247. doi: 10.1038/nprot.2006.164
52. Deitmer, J. W., and Rose, C. R. (2010). Ion changes and signalling in perisynaptic glia. Brain Res. Rev. 63, 113-129. doi: 10.1016/j.brainresrev.2009.10.006
53. De Pina-Benabou, M. H., Srinivas, M., Spray, D. C., and Scemes, E. (2001). Calmodulin kinase pathway mediates the K+-induced increase in Gap junctional communication between mouse spinal cord astrocytes. J. Neurosci. 21, 6635-6643.
54. De Saint Jan, D. (2005). Detecting activity in olfactory bulb glomeruli with astrocyte recording. J. Neurosci. 25, 2917-2924. doi: 10.1523/JNEUROSCI.5042-04.2005
55. Di Castro, M. A., Chuquet, J., Liaudet, N., Bhaukaurally, K., Santello, M., Bouvier, D., et al. (2011). Local Ca2+ detection and modulation of synaptic release by astrocytes. Nat. Neurosci. 14, 1276-1284. doi: 10.1038/nn.2929
56. Diamond, J. S. (2005). Deriving the glutamate clearance time course from transporter currents in CA1 hippocampal astrocytes: transmitter uptake gets faster during development. J. Neurosci. 25, 2906-2916. doi: 10.1523/JNEUROSCI.5125-04.2005
57. Diamond, J. S., Bergles, D. E., and Jahr, C. E. (1998). Glutamate release monitored with astrocyte transporter currents during LTP. Neuron 21, 425-433. doi: 10.1016/S0896-6273(00)80551-6
58. Djukic, B., Casper, K. B., Philpot, B. D., Chin, L.-S., and McCarthy, K. D. (2007). Conditional knock-out of Kir4.1 leads to glial membrane depolarization, inhibition of potassium and glutamate uptake, and enhanced short-term synaptic potentiation. J. Neurosci. 27, 11354-11365. doi: 10.1523/JNEUROSCI.0723-07.2007
59. Dufour, S., Dufour, P., Chever, O., Vallée, R., and Amzica, F. (2011). In vivosimultaneous intra-and extracellular potassium recordings using a micro-optrode. J. Neurosci. Methods 194, 206-217. doi: 10.1016/j.jneumeth.2010.10.004
60. Enkvist, M. O., and McCarthy, K. D. (1994). Astroglial gap junction communication is increased by treatment with either glutamate or high K+ concentration. J. Neurochem. 62, 489-495. doi: 10.1046/j.1471-4159.1994.62020489.x
61. Fellin, T., Pascual, O., Gobbo, S., Pozzan, T., Haydon, P. G., and Carmignoto, G. (2004). Neuronal synchrony mediated by astrocytic glutamate through activation of extrasynaptic NMDA receptors. Neuron 43, 729-743. doi: 10.1016/j.neuron.2004.08.011
62. Fiacco, T. A., Agulhon, C., Taves, S. R., Petravicz, J., Casper, K. B., Dong, X., et al. (2007). Selective stimulation of astrocyte calcium in situ does not affect neuronal excitatory synaptic activity. Neuron 54, 611-626. doi: 10.1016/j.neuron.2007.04.032
63. Fiacco, T. A., and McCarthy, K. D. (2004). Intracellular astrocyte calcium waves in situ increase the frequency of spontaneous AMPA receptor currents in CA1 pyramidal neurons. J. Neurosci. 24, 722-732. doi: 10.1523/JNEUROSCI.2859-03.2004
64. Floyd, C. L., Gorin, F. A., and Lyeth, B. G. (2005). Mechanical strain injury increases intracellular sodium and reverses Na+/Ca2+ exchange in cortical astrocytes. Glia 51, 35-46. doi: 10.1002/glia.20183
65. Förstl, J., Galvan, M., and ten Bruggencate, G. (1982). Extracellular K+ concentration during electrical stimulation of rat isolated sympathetic ganglia, vagus and optic nerves. Neuroscience 7, 3221-3229. doi: 10.1016/0306-4522(82)90244-5
66. Gabriel, S., Kivi, A., Eilers, A., Kovács, R., and Heinemann, U. (1998). Effects of barium on stimulus-induced rises in [K+]o in juvenile rat hippocampal area CA1. Neuroreport9, 2583-2587. doi: 10.1097/00001756-199808030-00029
67. Ge, W.-P., and Duan, S. (2007). Persistent enhancement of neuron-glia signaling mediated by increased extracellular K+ accompanying long-term synaptic potentiation. J. Neurophysiol. 97, 2564-2569. doi: 10.1152/jn.00146.2006
68. Genoud, C., Quairiaux, C., Steiner, P., Hirling, H., Welker, E., and Knott, G. W. (2006). Plasticity of astrocytic coverage and glutamate transporter expression in adult mouse cortex. PLoS Biol. 4:e343. doi: 10.1371/journal.pbio.0040343
69. Giaume, C., Fromaget, C., el Aoumari, A., Cordier, J., Glowinski, J., and Gros, D. (1991). Gap junctions in cultured astrocytes: single-channel currents and characterization of channel-forming protein. Neuron 6, 133-143. doi: 10.1016/0896-6273(91)90128-M
70. Giaume, C., Koulakoff, A., Roux, L., Holcman, D., and Rouach, N. (2010). Astroglial networks: a step further in neuroglial and gliovascular interactions. Nat. Rev. Neurosci. 11, 87-99. doi: 10.1038/nrn2757
71. Giaume, C., Orellana, J. A., Abudara, V., and Sáez, J. C. (2012). Connexin-based channels in astrocytes: how to study their properties. Methods Mol. Biol. 814, 283-303. doi: 10.1007/978-1-61779-452-0_19
72. Gómez-Gonzalo, M., Losi, G., Chiavegato, A., Zonta, M., Cammarota, M., Brondi, M., et al. (2010). An excitatory loop with astrocytes contributes to drive neurons to seizure threshold. PLoS Biol. 8:e1000352. doi: 10.1371/journal.pbio.1000352
73. Goubard, V., Fino, E., and Venance, L. (2011). Contribution of astrocytic glutamate and GABA uptake to corticostriatal information processing. J. Physiol. 589, 2301-2319. doi: 10.1113/jphysiol.2010.203125
74. Grass, D., Pawlowski, P. G., Hirrlinger, J., Papadopoulos, N., Richter, D. W., Kirchhoff, F., et al. (2004). Diversity of functional astroglial properties in the respiratory network. J. Neurosci. 24, 1358-1365. doi: 10.1523/JNEUROSCI.4022-03.2004
75. Grimaldi, M., Atzori, M., Ray, P., and Alkon, D. L. (2001). Mobilization of calcium from intracellular stores, potentiation of neurotransmitter-induced calcium transients, and capacitative calcium entry by 4-aminopyridine. J. Neurosci. 21, 3135-3143.
76. Haj-Yasein, N. N., Jensen, V., Vindedal, G. F., Gundersen, G. A., Klungland, A., Ottersen, O. P., et al. (2011). Evidence that compromised K+ spatial buffering contributes to the epileptogenic effect of mutations in the human Kir4.1 gene (KCNJ10). Glia 59, 1635-1642. doi: 10.1002/glia.21205
77. Hamilton, N. B., and Attwell, D. (2010). Do astrocytes really exocytose neurotransmitters? Nat. Rev. Neurosci. 11, 227-238. doi: 10.1038/nrn2803
78. Han, X., Chen, M., Wang, F., Windrem, M., Wang, S., Shanz, S., et al. (2013). Forebrain engraftment by human glial progenitor cells enhances synaptic plasticity and learning in adult mice. Cell Stem Cell 12, 342-353. doi: 10.1016/j.stem.2012.12.015
79. Hawrylak, N., Chang, F. L., and Greenough, W. T. (1993). Astrocytic and synaptic response to kindling in hippocampal subfield CA1. II. Synaptogenesis and astrocytic process increases to in vivo kindling. Brain Res. 603, 309-316. doi: 10.1016/0006-8993(93)91253-O
80. Henneberger, C., Papouin, T., Oliet, S. H. R., Dmitri, A., and Rusakov, D. A. (2010). Long-term potentiation depends on release of D-serine from astrocytes. Nature 463, 232-236. doi: 10.1038/nature08673
81. Henneberger, C., and Rusakov, D. A. (2012). Monitoring local synaptic activity with astrocytic patch pipettes. Nat. Protoc. 7, 2171-2179. doi: 10.1038/nprot.2012.140
82. Hibino, H. (2004). Differential assembly of inwardly rectifying K+ channel subunits, Kir4.1 and Kir5.1, in brain astrocytes. J. Biol. Chem. 279, 44065-44073. doi: 10.1074/jbc.M405985200
83. Higashi, K., Fujita, A., Inanobe, A., Tanemoto, M., Doi, K., Kubo, T., et al. (2001). An inwardly rectifying K(+) channel, Kir4.1, expressed in astrocytes surrounds synapses and blood vessels in brain. Am. J. Physiol. Cell Physiol. 281, C922-C931.
84. Huang, Y. H., and Bergles, D. E. (2004). Glutamate transporters bring competition to the synapse. Curr. Opin. Neurobiol. 14, 346-352. doi: 10.1016/j.conb.2004.05.007
85. Huang, Y. H., Sinha, S. R., Tanaka, K., Rothstein, J. D., and Bergles, D. E. (2004). Astrocyte glutamate transporters regulate metabotropic glutamate receptor-mediated excitation of hippocampal interneurons. J. Neurosci. 24, 4551-4559. doi: 10.1523/JNEUROSCI.5217-03.2004
86. Innocenti, B., Parpura, V., and Haydon, P. G. (2000). Imaging extracellular waves of glutamate during calcium signaling in cultured astrocytes. J. Neurosci. 20, 1800-1808.
87. Isokawa, M., and McKhann, G. M. (2005). Electrophysiological and morphological characterization of dentate astrocytes in the hippocampus. J. Neurobiol. 65, 125-134. doi: 10.1002/neu.20186
88. Jabaudon, D., Scanziani, M., Gahwiler, B. H., and Gerber, U. (2000). Acute decrease in net glutamate uptake during energy deprivation. Proc. Natl. Acad. Sci. U.S.A. 97, 5610-5615. doi: 10.1073/pnas.97.10.5610
89. Jabs, R., Seifert, G., and Steinhäuser, C. (2008). Astrocytic function and its alteration in the epileptic brain. Epilepsia 49(Suppl. 2), 3-12. doi: 10.1111/j.1528-1167.2008.01488.x
90. Jauch, R., Windmüller, O., Lehmann, T.-N., Heinemann, U., and Gabriel, S. (2002). Effects of barium, furosemide, ouabaine and 4,4'-diisothiocyanatostilbene-2,2'-disulfonic acid (DIDS) on ionophoretically-induced changes in extracellular potassium concentration in hippocampal slices from rats and from patients with epilepsy. Brain Res. 925, 18-27. doi: 10.1016/S0006-8993(01)03254-1
91. Jones, T. A., and Greenough, W. T. (1996). Ultrastructural evidence for increased contact between astrocytes and synapses in rats reared in a complex environment. Neurobiol. Learn. Mem. 65, 48-56. doi: 10.1006/nlme.1996.0005
92. Kafitz, K. W., Meier, S. D., Stephan, J., and Rose, C. R. (2008). Developmental profile and properties of sulforhodamine 101-Labeled glial cells in acute brain slices of rat hippocampus. J. Neurosci. Methods 169, 84-92. doi: 10.1016/j.jneumeth.2007.11.022
93. Kalsi, A. S., Greenwood, K., Wilkin, G., and Butt, A. M. (2004). Kir4.1 expression by astrocytes and oligodendrocytes in CNS white matter: a developmental study in the rat optic nerve. J. Anat. 204, 475-485. doi: 10.1111/j.0021-8782.2004.00288.x
94. Kang, J., Jiang, L., Goldman, S. A., and Nedergaard, M. (1998). Astrocyte-mediated potentiation of inhibitory synaptic transmission. Nat. Neurosci. 1, 683-692. doi: 10.1038/3684
95. Kang, N., Xu, J., Xu, Q., Nedergaard, M., and Kang, J. (2005). Astrocytic glutamate release-induced transient depolarization and epileptiform discharges in hippocampal CA1 pyramidal neurons. J. Neurophysiol. 94, 4121-4130. doi: 10.1152/jn.00448.2005
96. Karahashi, Y., and Goldring, S. (1966). Intracellular potentials from "idle" cells in cerebral cortex of cat. Electroencephalogr. Clin. Neurophysiol. 20, 600-607. doi: 10.1016/0013-4694(66)90024-1
97. Karwoski, C. J., Coles, J. A., Lu, H. K., and Huang, B. (1989). Current-evoked transcellular K+ flux in frog retina. J. Neurophysiol. 61, 939-952.
98. Kirischuk, S., Kettenmann, H., and Verkhratsky, A. (2007). Membrane currents and cytoplasmic sodium transients generated by glutamate transport in Bergmann glial cells. Pflügers Arch. Eur. J. Physiol. 454, 245-252. doi: 10.1007/s00424-007-0207-5
99. 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
100. Kozlov, A. S., Angulo, M. C., Audinat, E., and Charpak, S. (2006). Target cell-specific modulation of neuronal activity by astrocytes. Proc. Natl. Acad. Sci. U.S.A. 103, 10058-10063. doi: 10.1073/pnas.0603741103
101. Kressin, K., Kuprijanova, E., Jabs, R., Seifert, G., and Steinhäuser, C. (1995). Developmental regulation of Na+ and K+ conductances in glial cells of mouse hippocampal brain slices. Glia 15, 173-187. doi: 10.1002/glia.440150210
102. Kroeger, D., and Amzica, F. (2007). Hypersensitivity of the anesthesia-induced comatose brain. J. Neurosci. 27, 10597-10607. doi: 10.1523/JNEUROSCI.3440-07.2007
103. Kucheryavykh, Y. V., Kucheryavykh, L. Y., Nichols, C. G., Maldonado, H. M., Baksi, K., Reichenbach, A., et al. (2007). Downregulation of Kir4.1 inward rectifying potassium channel subunits by RNAi impairs potassium transfer and glutamate uptake by cultured cortical astrocytes. Glia 55, 274-281. doi: 10.1002/glia.20455
104. Kuffler, S. W., Nicholls, J. G., and Orkand, R. K. (1966). Physiological properties of glial cells in the central nervous system of amphibia. J. Neurophysiol. 29, 768-787.
105. Kuga, N., Sasaki, T., Takahara, Y., Matsuki, N., and Ikegaya, Y. (2011). Large-scale calcium waves traveling through astrocytic networks in vivo. J. Neurosci. 31, 2607-2614. doi: 10.1523/JNEUROSCI.5319-10.2011
106. Langer, J., Stephan, J., Theis, M., and Rose, C. R. (2012). Gap junctions mediate intercellular spread of sodium between hippocampal astrocytes in situ. Glia 60, 239-252. doi: 10.1002/glia.21259
107. Levy, L. M., Warr, O., and Attwell, D. (1998). Stoichiometry of the glial glutamate transporter GLT-1 expressed inducibly in a chinese hamster ovary cell line selected for low endogenous Na+-dependent glutamate uptake. J. Neurosci. 18, 9620-9628.
108. Lin, S.-C., and Bergles, D. E. (2002). Physiological characteristics of NG2-expressing glial cells. J. Neurocytol. 31, 537-549. doi: 10.1023/A:1025799816285
109. Linden, D. J. (1997). Long-term potentiation of glial synaptic currents in cerebellar culture. Neuron 18, 983-994. doi: 10.1016/S0896-6273(00)80337-2
110. Lüscher, C., Malenka, R. C., and Nicoll, R. A. (1998). Monitoring glutamate release during LTP with glial transporter currents. Neuron 21, 435-441. doi: 10.1016/S0896-6273(00)80552-8
111. Lushnikova, I., Skibo, G., Muller, D., and Nikonenko, I. (2009). Synaptic potentiation induces increased glial coverage of excitatory synapses in CA1 hippocampus. Hippocampus 19, 753-762. doi: 10.1002/hipo.20551
112. MacFarlane, S. N., and Sontheimer, H. (1997). Electrophysiological changes that accompany reactive gliosis in vitro. J. Neurosci. 17, 7316-7329.
113. MacVicar, B. A., Feighan, D., Brown, A., and 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. doi: 10.1002/glia.10023
114. MacVicar, B. A., and Hochman, D. (1991). Imaging of synaptically evoked intrinsic optical signals in hippocampal slices. J. Neurosci. 11, 1458-1469.
115. Maldonado, P. P., Vélez-Fort, M., Levavasseur, F., and Angulo, M. C. (2013). Oligodendrocyte precursor cells are accurate sensors of local K+ in mature gray matter. J. Neurosci. 33, 2432-2442. doi: 10.1523/JNEUROSCI.1961-12.2013
116. Matthias, K., Kirchhoff, F., Seifert, G., Hüttmann, K., Matyash, M., Kettenmann, H., et al. (2003). Segregated expression of AMPA-type glutamate receptors and glutamate transporters defines distinct astrocyte populations in the mouse hippocampus. J. Neurosci. 23, 1750-1758.
117. Meeks, J. P., and Mennerick, S. (2007). Astrocyte membrane responses and potassium accumulation during neuronal activity. Hippocampus 17, 1100-1108. doi: 10.1002/hipo.20344
118. Même, W., Vandecasteele, M., Giaume, C., and Venance, L. (2009). Electrical coupling between hippocampal astrocytes in rat brain slices. Neurosci. Res. 63, 236-243. doi: 10.1016/j.neures.2008.12.008
119. Mennerick, S., and Zorumski, C. F. (1994). Glial contributions to excitatory neurotransmission in cultured hippocampal cells. Nature 368, 59-62. doi: 10.1038/368059a0
120. Minelli, A., Barbaresi, P., Reimer, R., Edwards, R., and Conti, F. (2001). The glial glutamate transporter GLT-1 is localized both in the vicinity of and at distance from axon terminals in the rat cerebral cortex. Neuroscience 108, 51-59. doi: 10.1016/S0306-4522(01)00375-X
121. Mishima, T., and Hirase, H. (2010). In vivo intracellular recording suggests that gray matter astrocytes in mature cerebral cortex and hippocampus are electrophysiologically homogeneous. J. Neurosci. 30, 3093-3100. doi: 10.1523/JNEUROSCI.5065-09.2010
122. Mishima, T., Sakatani, S., and Hirase, H. (2007). Intracellular labeling of single cortical astrocytes in vivo. J. Neurosci. Methods 166, 32-40. doi: 10.1016/j.jneumeth.2007.06.021
123. Molenaar, R. J. (2011). Ion channels in glioblastoma. Isrn Neurol. 2011:590249. doi: 10.5402/2011/590249
124. Müller, M., and Somjen, G. G. (2000). Na+ and K+ concentrations, extra-and intracellular voltages, and the effect of TTX in hypoxic rat hippocampal slices. J. Neurophysiol. 83, 735-745.
125. Murphy, T. H., and Wier, W. G. (1993). Rapid communication between neurons and astrocytes in primary cortical cultures. J. Neurosci. 13, 2672-2679.
126. Navarrete, M., and Araque, A. (2008). Endocannabinoids mediate neuron-astrocyte communication. Neuron 57, 883-893. doi: 10.1016/j.neuron.2008.01.029
127. Navarrete, M., and Araque, A. (2010). Endocannabinoids potentiate synaptic transmission through stimulation of astrocytes. Neuron 68, 113-126. doi: 10.1016/j.neuron.2010.08.043
128. Navarrete, M., Perea, G., Maglio, L., Pastor, J., García de Sola, R., and Araque, A. (2012). Astrocyte calcium signal and gliotransmission in human brain tissue. Cereb. Cortex 23, 1240-1246. doi: 10.1093/cercor/bhs122
129. Nedergaard, M., and Verkhratsky, A. (2012). Artifact versus reality-how astrocytes contribute to synaptic events. Glia 60, 1013-1023. doi: 10.1002/glia.22288
130. Neusch, C., Papadopoulos, N., Müller, M., Maletzki, I., Winter, S. M., Hirrlinger, J., et al. (2006). Lack of the Kir4.1 channel subunit abolishes K+ buffering properties of astrocytes in the ventral respiratory group: impact on extracellular K+ regulation. J. Neurophysiol. 95, 1843-1852. doi: 10.1152/jn.00996.2005
131. Newman, E., and Reichenbach, A. (1996). The Müller cell: a functional element of the retina. Trends Neurosci. 19, 307-312. doi: 10.1016/0166-2236(96)10040-0
132. Newman, E. A. (2003). New roles for astrocytes: regulation of synaptic transmission. Trends Neurosci. 26, 536-542. doi: 10.1016/S0166-2236(03)00237-6
133. Nixdorf-Bergweiler, B. E., Albrecht, D., and Heinemann, U. (1994). Developmental changes in the number, size, and orientation of GFAP-positive cells in the CA1 region of rat hippocampus. Glia 12, 180-195. doi: 10.1002/glia.440120304
134. O'Connor, E. R., Sontheimer, H., Spencer, D. D., and de Lanerolle, N. C. (1998). Astrocytes from human hippocampal epileptogenic foci exhibit action potential-like responses. Epilepsia 39, 347-354. doi: 10.1111/j.1528-1157.1998.tb01386.x
135. Oliet, S. H., Piet, R., and Poulain, D. A. (2001). Control of glutamate clearance and synaptic efficacy by glial coverage of neurons. Science 292, 923-926. doi: 10.1126/science.1059162
136. Oliet, S. H. R., and Bonfardin, V. D. J. (2010). Morphological plasticity of the rat supraoptic nucleus-cellular consequences. Eur. J. Neurosci. 32, 1989-1994. doi: 10.1111/j.1460-9568.2010.07514.x
137. Olsen, M. (2012). "Examining potassium channel function in astrocytes, " in Methods in Molecular Biology, ed J. M. Walker (Clifton, NJ: Humana Press), 265. doi: 10.1007/978-1-61779-452-0_18
138. Olsen, M. L., Higashimori, H., Campbell, S. L., Hablitz, J. J., and Sontheimer, H. (2006). Functional expression of Kir4.1 channels in spinal cord astrocytes. Glia 53, 516-528. doi: 10.1002/glia.20312
139. Olsen, M. L., and Sontheimer, H. (2008). Functional implications for Kir4.1 channels in glial biology: from K+ buffering to cell differentiation. J. Neurochem. 107, 589-601. doi: 10.1111/j.1471-4159.2008.05615.x
140. Orkand, R. K., Nicholls, J. G., and Kuffler, S. W. (1966). Effect of nerve impulses on the membrane potential of glial cells in the central nervous system of amphibia. J. Neurophysiol. 29, 788-806.
141. Owe, S. G., Marcaggi, P., and Attwell, D. (2006). The ionic stoichiometry of the GLAST glutamate transporter in salamander retinal glia. J. Physiol. 577, 591-599. doi: 10.1113/jphysiol.2006.116830
142. Panatier, A., Vallée, J., Haber, M., Murai, K. K., Lacaille, J.-C., and Robitaille, R. (2011). Astrocytes are endogenous regulators of basal transmission at central synapses. Cell 146, 785-798. doi: 10.1016/j.cell.2011.07.022
143. Pannasch, U., Derangeon, M., Chever, O., and Rouach, N. (2012a). Astroglial gap junctions shape neuronal network activity. Commun. Integr. Biol. 5, 248-254. doi: 10.4161/cib.19410
144. Pannasch, U., Sibille, J., and Rouach, N. (2012b). Dual electrophysiological recordings of synaptically-evoked astroglial and neuronal responses in acute hippocampal slices.J. Vis. Exp. 69:e4418. doi: 10.3791/4418
145. Pannasch, U., Vargová, L., Reingruber, J., Ezan, P., Holcman, D., Giaume, C., et al. (2011). Astroglial networks scale synaptic activity and plasticity. Proc. Natl. Acad. Sci. U.S.A. 108, 8467-8472. doi: 10.1073/pnas.1016650108
146. Parpura, V., and Haydon, P. G. (2000). Physiological astrocytic calcium levels stimulate glutamate release to modulate adjacent neurons. Proc. Natl. Acad. Sci. U.S.A. 97, 8629-8634. doi: 10.1073/pnas.97.15.8629
147. Parri, H. R., Gould, T. M., and Crunelli, V. (2010). Sensory and cortical activation of distinct glial cell subtypes in the somatosensory thalamus of young rats. Eur. J. Neurosci. 32, 29-40. doi: 10.1111/j.1460-9568.2010.07281.x
148. Päsler, D., Gabriel, S., and Heinemann, U. (2007). Two-pore-domain potassium channels contribute to neuronal potassium release and glial potassium buffering in the rat hippocampus. Brain Res. 1173, 14-26. doi: 10.1016/j.brainres.2007.07.013
149. Pellerin, L., and Magistretti, P. J. (1994). Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization. Proc. Natl. Acad. Sci. U.S.A. 91, 10625-10629. doi: 10.1073/pnas.91.22.10625
150. Pellerin, L., and Magistretti, P. J. (2012). Sweet sixteen for ANLS. J. Cereb. Blood Flow Metab. Off. J. Int. Soc. Cereb. Blood Flow Metab. 32, 1152-1166. doi: 10.1038/jcbfm.2011.149
151. Perea, G., Navarrete, M., and Araque, A. (2009). Tripartite synapses: astrocytes process and control synaptic information. Trends Neurosci. 32, 421-431. doi: 10.1016/j.tins.2009.05.001
152. Petravicz, J., Fiacco, T. A., and McCarthy, K. D. (2008). Loss of IP3 receptor-dependent Ca2+ increases in hippocampal astrocytes does not affect baseline CA1 pyramidal neuron synaptic activity. J. Neurosci. 28, 4967-4973. doi: 10.1523/JNEUROSCI.5572-07.2008
153. Phillips, C. G. (1956). Intracellular records from Betz cells in the cat. Q. J. Exp. Physiol. Cogn. Med. Sci. 41, 58-69.
154. Piet, R., Vargová, L., Syková, E., Poulain, D. A., and Oliet, S. H. R. (2004). Physiological contribution of the astrocytic environment of neurons to intersynaptic crosstalk. Proc. Natl. Acad. Sci. U.S.A. 101, 2151-2155. doi: 10.1073/pnas.0308408100
155. Poolos, N. P., Mauk, M. D., and Kocsis, J. D. (1987). Activity-evoked increases in extracellular potassium modulate presynaptic excitability in the CA1 region of the hippocampus. J. Neurophysiol. 58, 404-416.
156. Proper, E. A, Hoogland, G., Kappen, S. M., Jansen, G. H., Rensen, M. G. A, Schrama, L. H., et al. (2002). Distribution of glutamate transporters in the hippocampus of patients with pharmaco-resistant temporal lobe epilepsy. Brain J. Neurol. 125, 32-43. doi: 10.1093/brain/awf001
157. Pumain, R., and Heinemann, U. (1985). Stimulus-and amino acid-induced calcium and potassium changes in rat neocortex. J. Neurophysiol. 53, 1-16.
158. Richardson, W. D., Young, K. M., Tripathi, R. B., and McKenzie, I. (2011). NG2-glia as multipotent neural stem cells: fact or fantasy? Neuron 70, 661-673. doi: 10.1016/j.neuron.2011.05.013
159. Ransom, B. R., and Goldring, S. (1973). Slow hyperpolarization in cells presumed to be glia in cerebral cortex of cat. J. Neurophysiol. 36, 879-892.
160. Ransom, B. R., Yamate, C. L., and Connors, B. W. (1985). Activity-dependent shrinkage of extracellular space in rat optic nerve: a developmental study. J. Neurosci. 5, 532-535.
161. Ransom, C. B., O'Neal, J. T., and Sontheimer, H. (2001). Volume-activated chloride currents contribute to the resting conductance and invasive migration of human glioma cells. J. Neurosci. 21, 7674-7683.
162. Ransom, C. B., Ransom, B. R., and Sontheimer, H. (2000). Activity-dependent extracellular K+ accumulation in rat optic nerve: the role of glial and axonal Na+ pumps. J. Physiol. 522(Pt 3), 427-442. doi: 10.1111/j.1469-7793.2000.00427.x
163. Raz-prag, D., Grimes, W. N., Fariss, R. N., Vijayasarathy, C., and Campos, M. M. (2010). Probing potassium channel function in vivo by intracellular delivery of antibodies in a rat model of retinal neurodegeneration. Proc. Natl. Acad. Sci. U.S.A. 107, 12710. doi: 10.1073/pnas.0913472107
164. Rothstein, J. D., Martin, L., Levey, A. I., Dykes-Hoberg, M., Jin, L., Wu, D., et al. (1994). Localization of neuronal and glial glutamate transporters. Neuron 13, 713-725. doi: 10.1016/0896-6273(94)90038-8
165. Rouach, N., Koulakoff, A., Abudara, V., Willecke, K., and Giaume, C. (2008). Astroglial metabolic networks sustain hippocampal synaptic transmission. Science 322, 1551-1555. doi: 10.1126/science.1164022
166. Roux, L., Benchenane, K., Rothstein, J. D., Bonvento, G., and Giaume, C. (2011). Plasticity of astroglial networks in olfactory glomeruli. Proc. Natl. Acad. Sci. U.S.A. 108, 18442-18446. doi: 10.1073/pnas.1107386108
167. Ruminot, I., Gutiérrez, R., Peña-Münzenmayer, G., Añazco, C., Sotelo-Hitschfeld, T., Lerchundi, R., et al. (2011). NBCe1 mediates the acute stimulation of astrocytic glycolysis by extracellular K+. J. Neurosci. 31, 14264-14271. doi: 10.1523/JNEUROSCI.2310-11.2011
168. Santello, M., Bezzi, P., and Volterra, A. (2011). TNFα controls glutamatergic gliotransmission in the hippocampal dentate gyrus. Neuron 69, 988-1001. doi: 10.1016/j.neuron.2011.02.003
169. Santello, M., and Volterra, A. (2012). TNFα in synaptic function: switching gears. Trends Neurosci. 35, 638-647. doi: 10.1016/j.tins.2012.06.001
170. Schools, G. P., Zhou, M., and Kimelberg, H. K. (2006). Development of gap junctions in hippocampal astrocytes: evidence that whole cell electrophysiological phenotype is an intrinsic property of the individual cell. J. Neurophysiol. 96, 1383-1392. doi: 10.1152/jn.00449.2006
171. Schröder, W., Hinterkeuser, S., Seifert, G., Schramm, J., Jabs, R., Wilkin, G. P., et al. (2000). Functional and molecular properties of human astrocytes in acute hippocampal slices obtained from patients with temporal lobe epilepsy. Epilepsia41(Suppl. 6), S181-S184. doi: 10.1111/j.1528-1157.2000.tb01578.x
172. Schröder, W., Seifert, G., Hüttmann, K., Hinterkeuser, S., and Steinhäuser, C. (2002). AMPA receptor-mediated modulation of inward rectifier K+ channels in astrocytes of mouse hippocampus. Mol. Cell. Neurosci. 19, 447-458. doi: 10.1006/mcne.2001.1080
173. Scimemi, A., Tian, H., and Diamond, J. S. (2009). Neuronal transporters regulate glutamate clearance, NMDA receptor activation, and synaptic plasticity in the hippocampus. J. Neurosci. 29, 14581-14595. doi: 10.1523/JNEUROSCI.4845-09.2009
174. Seifert, G., Hüttmann, K., Binder, D. K., Hartmann, C., Wyczynski, A., Neusch, C., et al. (2009). Analysis of astroglial K+ channel expression in the developing hippocampus reveals a predominant role of the Kir4.1 subunit. J. Neurosci. 29, 7474-7488. doi: 10.1523/JNEUROSCI.3790-08.2009
175. Seigneur, J., Kroeger, D., Nita, D. A., and Amzica, F. (2006). Cholinergic action on cortical glial cells in vivo. Cereb. Cortex 16, 655-668. doi: 10.1093/cercor/bhj011
176. Shigetomi, E., Bowser, D. N., Sofroniew, M. V., and Khakh, B. S. (2008). Two forms of astrocyte calcium excitability have distinct effects on NMDA receptor-mediated slow inward currents in pyramidal neurons. J. Neurosci. 28, 6659-6663. doi: 10.1523/JNEUROSCI.1717-08.2008
177. Solessio, E., Linn, D. M., Perlman, I., and Lasater, E. M. (2000). Characterization with barium of potassium currents in turtle retinal Müller cells. J. Neurophysiol. 83, 418-430.
178. Somjen, G. G. (1975). Electrophysiology of neuroglia. Annu. Rev. Physiol. 37, 163-190. doi: 10.1146/annurev.ph.37.030175.001115
179. Somjen, G. G. (2002). Ion regulation in the brain: implications for pathophysiology. Neuroscientist 8, 254-267. doi: 10.1177/10758402008003011
180. Somjen, G. G., Kager, H., and Wadman, W. J. (2008). Computer simulations of neuron-glia interactions mediated by ion flux. J. Comput. Neurosci. 25, 349-365. doi: 10.1007/s10827-008-0083-9
181. Sontheimer, H. (1994). Voltage-dependent ion channels in glial cells. Glia 11, 156-172. doi: 10.1002/glia.440110210
182. Sontheimer, H., Black, J. A., and Waxman, S. G. (1996). Voltage-gated Na+ channels in glia: properties and possible functions. Trends Neurosci. 19, 325-331. doi: 10.1016/0166-2236(96)10039-4
183. Sontheimer, H., and Waxman, S. G. (1992). Ion channels in spinal cord astrocytes in vitro. II. Biophysical and pharmacological analysis of two Na+ current types. J. Neurophysiol. 68, 1001-1011.
184. Sontheimer, H., and Waxman, S. G. (1993). Expression of voltage-activated ion channels by astrocytes and oligodendrocytes in the hippocampal slice. J. Neurophysiol. 70, 1863-1873.
185. Steinhäuser, C., Jabs, R., and Kettenmann, H. (1994). Properties of GABA and glutamate responses in identified glial cells of the mouse hippocampal slice. Hippocampus 4, 19-35. doi: 10.1002/hipo.450040105
186. Steinhäuser, C., Seifert, G., and Deitmer, J. W. (2013). "Physiology of astrocytes: ions channels and ion transporters, " in Neuroglia, eds H. Kettenmann and B. R Ransom (New York, NY: Oxford University Press), 185.
187. Sugaya, E., Goldring, S., and O'Leary, J. L. (1964). Intracellular potentials associated with direct cortical response and seizure discharge in cat. Electroencephalogr. Clin. Neurophysiol. 17, 661-669. doi: 10.1016/0013-4694(64)90234-2
188. Sun, W., McConnell, E., Pare, J.-F., Xu, Q., Chen, M., Peng, W., et al. (2013). Glutamate-dependent neuroglial calcium signaling differs between young and adult brain. Science339, 197-200. doi: 10.1126/science.1226740
189. Tzingounis, A. V., and Wadiche, J. I. (2007). Glutamate transporters: confining runaway excitation by shaping synaptic transmission. Nat. Rev. Neurosci. 8, 935-947. doi: 10.1038/nrn2274
190. Unichenko, P., Myakhar, O., and Kirischuk, S. (2012). Intracellular Na+ concentration influences short-term plasticity of glutamate transporter-mediated currents in neocortical astrocytes. Glia 60, 605-614. doi: 10.1002/glia.22294
191. Verkhratsky, A., and Kettenmann, H. (1996). Calcium signalling in glial cells. Trends Neurosci. 19, 346-352. doi: 10.1016/0166-2236(96)10048-5
192. Verkhratsky, A., and Steinhäuser, C. (2000). Ion channels in glial cells. Brain Res. Brain Res. Rev. 32, 380-412. doi: 10.1016/S0165-0173(99)00093-4
193. Wallraff, A., Köhling, R., Heinemann, U., Theis, M., Willecke, K., and Steinhäuser, 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
194. Wallraff, A., Odermatt, B., Willecke, K., and Steinhäuser, C. (2004). Distinct types of astroglial cells in the hippocampus differ in gap junction coupling. Glia 48, 36-43. doi: 10.1002/glia.20040
195. Wang, X., Lou, N., Xu, Q., Tian, G.-F., Peng, W. G., Han, X., et al. (2006). Astrocytic Ca2+ signaling evoked by sensory stimulation in vivo. Nat. Neurosci. 9, 816-823. doi: 10.1038/nn1703
196. Wenzel, J., Lammert, G., Meyer, U., and Krug, M. (1991). The influence of long-term potentiation on the spatial relationship between astrocyte processes and potentiated synapses in the dentate gyrus neuropil of rat brain. Brain Res. 560, 122-131. doi: 10.1016/0006-8993(91)91222-M
197. Woo, D. H., Han, K.-S., Shim, J. W., Yoon, B.-E., Kim, E., Bae, J. Y., et al. (2012). TREK-1 and Best1 channels mediate fast and slow glutamate release in astrocytes upon GPCR activation. Cell 151, 25-40. doi: 10.1016/j.cell.2012.09.005
198. Xiong, Z. Q., and Stringer, J. L. (2000). Sodium pump activity, not glial spatial buffering, clears potassium after epileptiform activity induced in the dentate gyrus. J. Neurophysiol. 83, 1443-1451.
199. Xu, G., Wang, W., Kimelberg, H. K., and Zhou, M. (2010). Electrical coupling of astrocytes in rat hippocampal slices under physiological and simulated ischemic conditions. Glia 58, 481-493. doi: 10.1002/glia.20939
200. Zhang, H., Xin, W., and Dougherty, P. M. (2009). Synaptically evoked glutamate transporter currents in spinal dorsal horn astrocytes. Mol. Pain 5, 36. doi: 10.1186/1744-8069-5-36
201. Zhou, M. (2005). Development of GLAST(+) astrocytes and NG2(+) glia in rat hippocampus CA1: mature astrocytes are electrophysiologically passive. J. Neurophysiol. 95, 134-143. doi: 10.1152/jn.00570.2005
202. Zhou, M., Xu, G., Xie, M., Zhang, X., Schools, G. P., Ma, L., et al. (2009). TWIK-1 and TREK-1 are potassium channels contributing significantly to astrocyte passive conductance in rat hippocampal slices. J. Neurosci. 29, 8551-8564. doi: 10.1523/JNEUROSCI.5784-08.2009