Astrocytes convert network excitation to tonic inhibition of neurons

BMC Biology

Volumn 10, Issue , 2012, Pages

  Héja, László ^a   Nyitrai, Gabriella ^a   Kékesi, Orsolya ^a   Dobolyi, Árpád ^a   Szabó, Pál ^a   Fiáth, Richárd ^b   Ulbert, István ^b,c   Pál Szenthe, Borbála ^a   Palkovits, Miklós ^a   Kardos, Julianna ^a  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^b Research Centre for Natural Sciences Hungarian Academy of Sciences   (Hungary)

^c PÁZMÁNY PÉTER CATHOLIC UNIVERSITY   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID CARRIER; GLUTAMATE DECARBOXYLASE; GLUTAMATE TRANSPORTER; GLUTAMIC ACID;

ANIMAL; ARTICLE; ASTROCYTE; CYTOLOGY; DISEASE MODEL; EPILEPSY; FEEDBACK SYSTEM; HIPPOCAMPUS; HUMAN; METABOLISM; NERVE CELL INHIBITION; PATHOPHYSIOLOGY; RAT; SYNAPTIC TRANSMISSION; WISTAR RAT;

ANIMALS; ASTROCYTES; DISEASE MODELS, ANIMAL; EPILEPSY; FEEDBACK, PHYSIOLOGICAL; GABA PLASMA MEMBRANE TRANSPORT PROTEINS; GAMMA-AMINOBUTYRIC ACID; GLUTAMATE DECARBOXYLASE; GLUTAMATE PLASMA MEMBRANE TRANSPORT PROTEINS; GLUTAMIC ACID; HIPPOCAMPUS; HUMANS; NEURAL INHIBITION; RATS; RATS, WISTAR; SYNAPTIC TRANSMISSION;

EID: 84860426170     PISSN: None     EISSN: 17417007     Source Type: Journal    
DOI: 10.1186/1741-7007-10-26     Document Type: Article

References (88)

1. Perea G, Navarrete M, Araque A. Tripartite synapses: astrocytes process and control synaptic information. Trends Neurosci 2009, 32:421-431. 10.1016/j.tins.2009.05.001, 19615761.
2. Volterra A, Bezzi P. Release of transmitters from glial cells. Tripartite Synapse: Glia in SynapticTransmisson 2002, 164-182. Oxford, UK: Oxford University Press, Volterra A, Magistretti PJ, Haydon PG.
3. Schousboe A, Madsen KK, White HS. GABA transport inhibitors and seizure protection: the past and future. Future Med Chem 2011, 3:183-187. 10.4155/fmc.10.288, 21428813.
4. Danbolt NC. Glutamate uptake. Prog Neurobiol 2001, 65:1-105. 10.1016/S0301-0082(00)00067-8, 11369436.
5. Velez-Fort M, Audinat E, Angulo MC. Central role of GABA in neuron-glia interactions. Neuroscientist 2011,
6. Domingues AM, Taylor M, Fern R. Glia as transmitter sources and sensors in health and disease. Neurochem Int 2010, 57:359-366. 10.1016/j.neuint.2010.03.024, 20380859.
7. Madsen KK, Ebert B, Clausen RP, Krogsgaard-Larsen P, Schousboe A, White HS. Selective GABA transporter inhibitors tiagabine and EF1502 exhibit mechanistic differences in their ability to modulate the ataxia and anticonvulsant action of the extrasynaptic GABA(A) receptor agonist gaboxadol. J Pharmacol Exp Ther 2011, 338:214-219. 10.1124/jpet.111.179671, 21450931.
8. Biber K, Laurie DJ, Berthele A, Sommer B, Tolle TR, Gebicke-Harter PJ, van Calker D, Boddeke HW. Expression and signaling of group I metabotropic glutamate receptors in astrocytes and microglia. J Neurochem 1999, 72:1671-1680.
9. Doengi M, Hirnet D, Coulon P, Pape HC, Deitmer JW, Lohr C. GABA uptake-dependent Ca(2+) signaling in developing olfactory bulb astrocytes. Proc Natl Acad Sci USA 2009, 106:17570-17575. 10.1073/pnas.0809513106, 2765163, 19805126.
10. Haydon PG, Carmignoto G. Astrocyte control of synaptic transmission and neurovascular coupling. Physiol Rev 2006, 86:1009-1031. 10.1152/physrev.00049.2005, 16816144.
11. Hamilton NB, Attwell D. Do astrocytes really exocytose neurotransmitters?. Nat Rev Neurosci 2010, 11:227-238. 10.1038/nrn2803, 20300101.
12. Allen NJ, Rossi DJ, Attwell D. Sequential release of GABA by exocytosis and reversed uptake leads to neuronal swelling in simulated ischemia of hippocampal slices. J Neurosci 2004, 24:3837-3849. 10.1523/JNEUROSCI.5539-03.2004, 15084665.
13. Belelli D, Harrison NL, Maguire J, Macdonald RL, Walker MC, Cope DW. Extrasynaptic GABAA receptors: form, pharmacology, and function. J Neurosci 2009, 29:12757-12763. 10.1523/JNEUROSCI.3340-09.2009, 2784229, 19828786.
14. Semyanov A, Walker MC, Kullmann DM, Silver RA. Tonically active GABA A receptors: modulating gain and maintaining the tone. Trends Neurosci 2004, 27:262-269. 10.1016/j.tins.2004.03.005, 15111008.
15. Cope DW, Di Giovanni G, Fyson SJ, Orban G, Errington AC, Lorincz ML, Gould TM, Carter DA, Crunelli V. Enhanced tonic GABAA inhibition in typical absence epilepsy. Nat Med 2009, 15:1392-1398. 10.1038/nm.2058, 2824149, 19966779.
16. Clarkson AN, Huang BS, Macisaac SE, Mody I, Carmichael ST. Reducing excessive GABA-mediated tonic inhibition promotes functional recovery after stroke. Nature 2010, 468:305-309. 10.1038/nature09511, 3058798, 21048709.
17. Glykys J, Mody I. The main source of ambient GABA responsible for tonic inhibition in the mouse hippocampus. J Physiol 2007, 582:1163-1178. 10.1113/jphysiol.2007.134460, 2075237, 17525114.
18. Wu Y, Wang W, Richerson GB. The transmembrane sodium gradient influences ambient GABA concentration by altering the equilibrium of GABA transporters. J Neurophysiol 2006, 96:2425-2436. 10.1152/jn.00545.2006, 16870837.
19. Eulenburg V, Gomeza J. Neurotransmitter transporters expressed in glial cells as regulators of synapse function. Brain Res Rev 2010, 63:103-112. 10.1016/j.brainresrev.2010.01.003, 20097227.
20. Gutierrez R, Heinemann U. Co-existence of GABA and Glu in the hippocampal granule cells: implications for epilepsy. Curr Top Med Chem 2006, 6:975-978. 10.2174/156802606777323692, 16787272.
21. Héja L, Karacs K, Kardos J. Role for GABA and Glu plasma membrane transporters in the interplay of inhibitory and excitatory neurotransmission. Curr Top Med Chem 2006, 6:989-995. 10.2174/156802606777323656, 16787274.
22. Liang SL, Carlson GC, Coulter DA. Dynamic regulation of synaptic GABA release by the glutamate-glutamine cycle in hippocampal area CA1. J Neurosci 2006, 26:8537-8548. 10.1523/JNEUROSCI.0329-06.2006, 2471868, 16914680.
23. Somogyi J. Functional significance of co-localization of GABA and Glu in nerve terminals: a hypothesis. Curr Top Med Chem 2006, 6:969-973. 10.2174/156802606777323737, 16787271.
24. Héja L, Barabás P, Nyitrai G, Kékesi KA, Lasztóczi B, To{double acute}ke O, Tárkányi G, Madsen K, Schousboe A, Dobolyi A, Palkovits M, Kardos J. Glutamate uptake triggers transporter-mediated GABA release from astrocytes. PLoS One 2009, 4:e7153. 10.1371/journal.pone.0007153, 2744931, 19777062.
25. Minelli A, DeBiasi S, Brecha NC, Zuccarello LV, Conti F. GAT-3, a high-affinity GABA plasma membrane transporter, is localized to astrocytic processes, and it is not confined to the vicinity of GABAergic synapses in the cerebral cortex. J Neurosci 1996, 16:6255-6264.
26. Kinney GA, Spain WJ. Synaptically evoked GABA transporter currents in neocortical glia. J Neurophysiol 2002, 88:2899-2908. 10.1152/jn.00037.2002, 12466416.
27. Milton ID, Banner SJ, Ince PG, Piggott NH, Fray AE, Thatcher N, Horne CH, Shaw PJ. Expression of the glial glutamate transporter EAAT2 in the human CNS: an immunohistochemical study. Brain Res Mol Brain Res 1997, 52:17-31.
28. Proper EA, Hoogland G, Kappen SM, Jansen GH, Rensen MG, Schrama LH, van Veelen CW, van Rijen PC, van Nieuwenhuizen O, Gispen WH, de Graan PN. Distribution of glutamate transporters in the hippocampus of patients with pharmaco-resistant temporal lobe epilepsy. Brain 2002, 125:32-43. 10.1093/brain/awf001, 11834591.
29. Li Q, Lau A, Morris TJ, Guo L, Fordyce CB, Stanley EF. A syntaxin 1, Galpha(o), and N-type calcium channel complex at a presynaptic nerve terminal: analysis by quantitative immunocolocalization. J Neurosci 2004, 24:4070-4081. 10.1523/JNEUROSCI.0346-04.2004, 15102922.
30. Furness DN, Dehnes Y, Akhtar AQ, Rossi DJ, Hamann M, Grutle NJ, Gundersen V, Holmseth S, Lehre KP, Ullensvang K, Wojewodzic M, Zhou Y, Attwell D, Danbolt NC. A quantitative assessment of glutamate uptake into hippocampal synaptic terminals and astrocytes: new insights into a neuronal role for excitatory amino acid transporter 2 (EAAT2). Neuroscience 2008, 157:80-94. 10.1016/j.neuroscience.2008.08.043, 2775085, 18805467.
31. Conti F, Zuccarello LV, Barbaresi P, Minelli A, Brecha NC, Melone M. Neuronal, glial, and epithelial localization of gamma-aminobutyric acid transporter 2, a high-affinity gamma-aminobutyric acid plasma membrane transporter, in the cerebral cortex and neighboring structures. J Comp Neurol 1999, 409:482-494. 10.1002/(SICI)1096-9861(19990705)409:3<482::AID-CNE11>3.0.CO;2-O, 10379832.
32. Ransom CB, Wu Y, Richerson GB. Postdepolarization potentiation of GABAA receptors: a novel mechanism regulating tonic conductance in hippocampal neurons. J Neurosci 2010, 30:7672-7684. 10.1523/JNEUROSCI.0290-10.2010, 2902370, 20519542.
33. Lozovaya N, Melnik S, Tsintsadze T, Grebenyuk S, Kirichok Y, Krishtal O. Protective cap over CA1 synapses: extrasynaptic glutamate does not reach the postsynaptic density. Brain Res 2004, 1011:195-205. 10.1016/j.brainres.2004.03.023, 15157806.
34. Qian A, Johnson JW. Permeant ion effects on external Mg2+ block of NR1/2D NMDA receptors. J Neurosci 2006, 26:10899-10910. 10.1523/JNEUROSCI.3453-06.2006, 17050728.
35. Nyitrai G, Lasztóczi B, Kardos J. Glutamate uptake shapes low-[Mg2+] induced epileptiform activity in juvenile rat hippocampal slices. Brain Res 2010, 1309:172-178.
36. Mody I, Lambert JD, Heinemann U. Low extracellular magnesium induces epileptiform activity and spreading depression in rat hippocampal slices. J Neurophysiol 1987, 57:869-888.
37. Wahab A, Heinemann U, Albus K. Effects of gamma-aminobutyric acid (GABA) agonists and a GABA uptake inhibitor on pharmacoresistant seizure like events in organotypic hippocampal slice cultures. Epilepsy Res 2009, 86:113-123. 10.1016/j.eplepsyres.2009.05.008, 19535226.
38. Lehre KP, Danbolt NC. The number of glutamate transporter subtype molecules at glutamatergic synapses: chemical and stereological quantification in young adult rat brain. J Neurosci 1998, 18:8751-8757.
39. Kanner BI. Structure and function of sodium-coupled GABA and glutamate transporters. J Membr Biol 2006, 213:89-100. 10.1007/s00232-006-0877-5, 17417704.
40. Nimmerjahn A, Kirchhoff F, Kerr JN, Helmchen F. Sulforhodamine 101 as a specific marker of astroglia in the neocortex in vivo. Nat Methods 2004, 1:31-37. 10.1038/nmeth706, 15782150.
41. Matthias K, Kirchhoff F, Seifert G, Huttmann K, Matyash M, Kettenmann H, Steinhauser C. Segregated expression of AMPA-type glutamate receptors and glutamate transporters defines distinct astrocyte populations in the mouse hippocampus. J Neurosci 2003, 23:1750-1758.
42. Rose CR, Konnerth A. NMDA receptor-mediated Na+ signals in spines and dendrites. J Neurosci 2001, 21:4207-4214.
43. Ochi S, Lim JY, Rand MN, During MJ, Sakatani K, Kocsis JD. Transient presence of GABA in astrocytes of the developing optic nerve. Glia 1993, 9:188-198. 10.1002/glia.440090304, 8294149.
44. Caron PC, Kremzner LT, Cote LJ. GABA and its relationship to putrescine metabolism in the rat brain and pancreas. Neurochem Int 1987, 10:219-229. 10.1016/0197-0186(87)90131-8, 20501074.
45. Seiler N, Schmidt-Glenewinkel T, Sarhan S. On the formation of gamma-aminobutyric acid from putrescine in brain. J Biochem 1979, 86:277-278.
46. Najm I, el-Skaf G, Massicotte G, Vanderklish P, Lynch G, Baudry M. Changes in polyamine levels and spectrin degradation following kainate-induced seizure activity: effect of difluoromethylornithine. Exp Neurol 1992, 116:345-354. 10.1016/0014-4886(92)90013-G, 1587335.
47. Halonen T, Sivenius J, Miettinen R, Halmekyto M, Kauppinen R, Sinervirta R, Alakuijala L, Alhonen L, MacDonald E, Janne J, et al. Elevated seizure threshold and impaired spatial learning in transgenic mice with putrescine overproduction in the brain. Eur J Neurosci 1993, 5:1233-1239. 10.1111/j.1460-9568.1993.tb00978.x, 8281326.
48. Laschet J, Grisar T, Bureau M, Guillaume D. Characteristics of putrescine uptake and subsequent GABA formation in primary cultured astrocytes from normal C57BL/6J and epileptic DBA/2J mouse brain cortices. Neuroscience 1992, 48:151-157. 10.1016/0306-4522(92)90345-3, 1584419.
49. Gimenez-Llort L, Martinez E, Camon L, de Vera N. Concentration of putrescine in plasma, frontal cortex and hippocampus of rats after systemic administration of the convulsants N-methyl-D-aspartate, pentylentetrazol, picrotoxinine, lindane and 4-aminopyridine. Neurosci Lett 1996, 217:1-4.
50. Vivo M, Camon L, de Vera N, Martinez E. Extracellular putrescine content after acute excitotoxic brain damage in the rat. Neurosci Lett 2002, 330:74-78. 10.1016/S0304-3940(02)00733-4, 12213638.
51. Baskaya MK, Rao AM, Dogan A, Donaldson D, Gellin G, Dempsey RJ. Regional brain polyamine levels in permanent focal cerebral ischemia. Brain Res 1997, 744:302-308. 10.1016/S0006-8993(96)01116-X, 9102140.
52. Rothman DL, Petroff OA, Behar KL, Mattson RH. Localized 1H NMR measurements of gamma-aminobutyric acid in human brain in vivo. Proc Natl Acad Sci USA 1993, 90:5662-5666. 10.1073/pnas.90.12.5662, 46781, 8516315.
53. Nyitrai G, Kékesi KA, Juhász G. Extracellular level of GABA and Glu: in vivo microdialysis-HPLC measurements. Curr Top Med Chem 2006, 6:935-940. 10.2174/156802606777323674, 16787267.
54. Masuko T, Kusama-Eguchi K, Sakata K, Kusama T, Chaki S, Okuyama S, Williams K, Kashiwagi K, Igarashi K. Polyamine transport, accumulation, and release in brain. J Neurochem 2003, 84:610-617. 10.1046/j.1471-4159.2003.01558.x, 12558981.
55. Gilad GM, Gilad VH. Polyamine uptake, binding and release in rat brain. Eur J Pharmacol 1991, 193:41-46. 10.1016/0014-2999(91)90198-Y, 2050191.
56. Fellous JM, Rudolph M, Destexhe A, Sejnowski TJ. Synaptic background noise controls the input/output characteristics of single cells in an in vitro model of in vivo activity. Neuroscience 2003, 122:811-829. 10.1016/j.neuroscience.2003.08.027, 2928821, 14622924.
57. Montgomery SM, Buzsaki G. Gamma oscillations dynamically couple hippocampal CA3 and CA1 regions during memory task performance. Proc Natl Acad Sci USA 2007, 104:14495-14500. 10.1073/pnas.0701826104, 1964875, 17726109.
58. Kopell N, Ermentrout GB, Whittington MA, Traub RD. Gamma rhythms and beta rhythms have different synchronization properties. Proc Natl Acad Sci USA 2000, 97:1867-1872. 10.1073/pnas.97.4.1867, 26528, 10677548.
59. Senior TJ, Huxter JR, Allen K, O'Neill J, Csicsvari J. Gamma oscillatory firing reveals distinct populations of pyramidal cells in the CA1 region of the hippocampus. J Neurosci 2008, 28:2274-2286. 10.1523/JNEUROSCI.4669-07.2008, 18305260.
60. Colling SB, Stanford IM, Traub RD, Jefferys JG. Limbic gamma rhythms. I. Phase-locked oscillations in hippocampal CA1 and subiculum. J Neurophysiol 1998, 80:155-161.
61. Oren I, Mann EO, Paulsen O, Hajos N. Synaptic currents in anatomically identified CA3 neurons during hippocampal gamma oscillations in vitro. J Neurosci 2006, 26:9923-9934. 10.1523/JNEUROSCI.1580-06.2006, 17005856.
62. Richerson GB, Wu Y. Dynamic equilibrium of neurotransmitter transporters: not just for reuptake anymore. J Neurophysiol 2003, 90:1363-1374. 10.1152/jn.00317.2003, 12966170.
63. Wu Y, Wang W, Diez-Sampedro A, Richerson GB. Nonvesicular inhibitory neurotransmission via reversal of the GABA transporter GAT-1. Neuron 2007, 56:851-865. 10.1016/j.neuron.2007.10.021, 2156040, 18054861.
64. Farrant M, Nusser Z. Variations on an inhibitory theme: phasic and tonic activation of GABA(A) receptors. Nat Rev Neurosci 2005, 6:215-229. 10.1038/nrn1625, 15738957.
65. Penner R, Fleig A. The Mg2+ and Mg(2+)-nucleotide-regulated channel-kinase TRPM7. Handb Exp Pharmacol 2007, 313-328.
66. Doi T, Ueda Y, Tokumaru J, Willmore LJ. Molecular regulation of glutamate and GABA transporter proteins by clobazam during epileptogenesis in Fe(+++)-induced epileptic rats. Brain Res Mol Brain Res 2005, 142:91-96.
67. Ueda Y, Doi T, Nagatomo K, Tokumaru J, Takaki M, Willmore LJ. Effect of levetiracetam on molecular regulation of hippocampal glutamate and GABA transporters in rats with chronic seizures induced by amygdalar FeCl3 injection. Brain Res 2007, 1151:55-61.
68. Lee TS, Bjornsen LP, Paz C, Kim JH, Spencer SS, Spencer DD, Eid T, de Lanerolle NC. GAT1 and GAT3 expression are differently localized in the human epileptogenic hippocampus. Acta Neuropathol 2006, 111:351-363. 10.1007/s00401-005-0017-9, 16456667.
69. Jow F, Chiu D, Lim HK, Novak T, Lin S. Production of GABA by cultured hippocampal glial cells. Neurochem Int 2004, 45:273-283. 10.1016/j.neuint.2003.11.021, 15145543.
70. Moussa CE, Rae C, Bubb WA, Griffin JL, Deters NA, Balcar VJ. Inhibitors of glutamate transport modulate distinct patterns in brain metabolism. J Neurosci Res 2007, 85:342-350. 10.1002/jnr.21108, 17086545.
71. Kozlov AS, Angulo MC, Audinat E, Charpak S. Target cell-specific modulation of neuronal activity by astrocytes. Proc Natl Acad Sci USA 2006, 103:10058-10063. 10.1073/pnas.0603741103, 1502505, 16782808.
72. Liu QY, Schaffner AE, Chang YH, Maric D, Barker JL. Persistent activation of GABA(A) receptor/Cl(-) channels by astrocyte-derived GABA in cultured embryonic rat hippocampal neurons. J Neurophysiol 2000, 84:1392-1403.
73. Angulo MC, Le Meur K, Kozlov AS, Charpak S, Audinat E. GABA, a forgotten gliotransmitter. Prog Neurobiol 2008, 86:297-303. 10.1016/j.pneurobio.2008.08.002, 18786601.
74. Wu PH, Durden DA, Hertz L. Net production of gamma-aminobutyric acid in astrocytes in primary cultures determined by a sensitive mass spectrometric method. J Neurochem 1979, 32:379-390. 10.1111/j.1471-4159.1979.tb00361.x, 216775.
75. Baudry M, Shahi K, Gall C. Induction of ornithine decarboxylase in adult rat hippocampal slices. Brain Res 1988, 464:313-318.
76. Massieu L, Morales-Villagran A, Tapia R. Accumulation of extracellular glutamate by inhibition of its uptake is not sufficient for inducing neuronal damage: an in vivo microdialysis study. J Neurochem 1995, 64:2262-2272.
77. Massieu L, Tapia R. Glutamate uptake impairment and neuronal damage in young and aged rats in vivo. J Neurochem 1997, 69:1151-1160.
78. Montiel T, Camacho A, Estrada-Sanchez AM, Massieu L. Differential effects of the substrate inhibitor l-trans-pyrrolidine-2,4-dicarboxylate (PDC) and the non-substrate inhibitor DL-threo-beta-benzyloxyaspartate (DL-TBOA) of glutamate transporters on neuronal damage and extracellular amino acid levels in rat brain in vivo. Neuroscience 2005, 133:667-678. 10.1016/j.neuroscience.2004.11.020, 15890455.
79. During MJ, Ryder KM, Spencer DD. Hippocampal GABA transporter function in temporal-lobe epilepsy. Nature 1995, 376:174-177. 10.1038/376174a0, 7603569.
80. Lasztóczi B, Nyitrai G, Héja L, Kardos J. Synchronization of GABAergic inputs to CA3 pyramidal cells precedes seizure-like event onset in juvenile rat hippocampal slices. J Neurophysiol 2009, 102:2538-2553. 10.1152/jn.91318.2008, 19675286.
81. Glykys J, Peng Z, Chandra D, Homanics GE, Houser CR, Mody I. A new naturally occurring GABA(A) receptor subunit partnership with high sensitivity to ethanol. Nat Neurosci 2007, 10:40-48. 10.1038/nn1813, 17159992.
82. Gulyas AI, Szabo GG, Ulbert I, Holderith N, Monyer H, Erdelyi F, Szabo G, Freund TF, Hajos N. Parvalbumin-containing fast-spiking basket cells generate the field potential oscillations induced by cholinergic receptor activation in the hippocampus. J Neurosci 2010, 30:15134-15145. 10.1523/JNEUROSCI.4104-10.2010, 3044880, 21068319.
83. Ulbert I, Magloczky Z, Eross L, Czirjak S, Vajda J, Bognar L, Toth S, Szabo Z, Halasz P, Fabo D, Halgren E, Freund TF, Karmos G. In vivo laminar electrophysiology co-registered with histology in the hippocampus of patients with temporal lobe epilepsy. Exp Neurol 2004, 187:310-318. 10.1016/j.expneurol.2003.12.003, 15144857.
84. Csercsa R, Dombovari B, Fabo D, Wittner L, Eross L, Entz L, Solyom A, Rasonyi G, Szucs A, Kelemen A, Jakus R, Juhos V, Grand L, Magony A, Halász P, Freund TF, Maglóczky Z, Cash SS, Papp L, Karmos G, Halgren E, Ulbert I. Laminar analysis of slow wave activity in humans. Brain 2010, 133:2814-2829. 10.1093/brain/awq169, 3105490, 20656697.
85. Ulbert I, Halgren E, Heit G, Karmos G. Multiple microelectrode-recording system for human intracortical applications. J Neurosci Methods 2001, 106:69-79. 10.1016/S0165-0270(01)00330-2, 11248342.
86. Chatton JY, Pellerin L, Magistretti PJ. GABA uptake into astrocytes is not associated with significant metabolic cost: implications for brain imaging of inhibitory transmission. Proc Natl Acad Sci USA 2003, 100:12456-12461. 10.1073/pnas.2132096100, 218779, 14530410.
87. Sihra TS, Nicholls DG. 4-Aminobutyrate can be released exocytotically from guinea-pig cerebral cortical synaptosomes. J Neurochem 1987, 49:261-267. 10.1111/j.1471-4159.1987.tb03424.x, 3585335.
88. Eckstein JA, Ammerman GM, Reveles JM, Ackermann BL. Analysis of glutamine, glutamate, pyroglutamate, and GABA in cerebrospinal fluid using ion pairing HPLC with positive electrospray LC/MS/MS. J Neurosci Methods 2008, 171:190-196. 10.1016/j.jneumeth.2008.02.019, 18433876.