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Neural Plasticity
Volume 2012 (2012), Article ID 805830, 12 pages
http://dx.doi.org/10.1155/2012/805830
Review Article

GABA Metabolism and Transport: Effects on Synaptic Efficacy

Institute of Physiology and Pathophysiology, University of Heidelberg, 69120 Heidelberg, Germany

Received 14 November 2011; Accepted 19 December 2011

Academic Editor: Dirk Bucher

Copyright © 2012 Fabian C. Roth and Andreas Draguhn. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. Wolfe, A. R. Houweling, and M. Brecht, “Sparse and powerful cortical spikes,” Current Opinion in Neurobiology, vol. 20, no. 3, pp. 306–312, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  2. K. N. Hartman, S. K. Pal, J. Burrone, and V. N. Murthy, “Activity-dependent regulation of inhibitory synaptic transmission in hippocampal neurons,” Nature Neuroscience, vol. 9, no. 5, pp. 642–649, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  3. E. Schonfeld-Dado and M. Segal, “Activity-dependent survival of neurons in culture: a model of slow neurodegeneration,” Journal of Neural Transmission, vol. 116, no. 11, pp. 1363–1369, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  4. A. Maffei and G. G. Turrigiano, “Multiple modes of network homeostasis in visual cortical layer 2/3,” Journal of Neuroscience, vol. 28, no. 17, pp. 4377–4384, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  5. V. Kilman, M. C. W. Van Rossum, and G. G. Turrigiano, “Activity deprivation reduces miniature IPSC amplitude by decreasing the number of postsynaptic GABAA receptors clustered at neocortical synapses,” Journal of Neuroscience, vol. 22, no. 4, pp. 1328–1337, 2002. View at Scopus
  6. Y. Ben-Ari, “Cell death and synaptic reorganizations produced by seizures,” Epilepsia, vol. 42, no. 3, pp. 5–7, 2001. View at Publisher · View at Google Scholar · View at Scopus
  7. J.P. Adelman, J. Maylie, and P. Sah, “Small-conductance Ca2+-activated K+ channels: form and function,” Annual Review of Physiology, vol. 74, pp. 245–269, 2012.
  8. A. Marty, “The physiological role of calcium-dependent channels,” Trends in Neurosciences, vol. 12, no. 11, pp. 420–424, 1989. View at Scopus
  9. M. O. Cunningham, D. D. Pervouchine, C. Racca et al., “Neuronal metabolism governs cortical network response state,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 14, pp. 5597–5601, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  10. C. Huchzermeyer, K. Albus, H. J. Gabriel et al., “Gamma oscillations and spontaneous network activity in the hippocampus are highly sensitive to decreases in pO2 and concomitant changes in mitochondrial redox state,” Journal of Neuroscience, vol. 28, no. 5, pp. 1153–1162, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  11. H. Mohler, P. Malherbe, A. Draguhn, and J. G. Richards, “GABAA-receptors: structural requirements and sites of gene expression in mammalian brain,” Neurochemical Research, vol. 15, no. 2, pp. 199–207, 1990. View at Scopus
  12. M. Ferrante, M. Migliore, and G. A. Ascoli, “Feed-forward inhibition as a buffer of the neuronal input-output relation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 42, pp. 18004–18009, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  13. T. F. Freund and G. Buzsáki, “Interneurons of the Hippocampus,” Hippocampus, vol. 6, no. 4, pp. 347–470, 1996. View at Scopus
  14. M. G. Maltenfort, C. J. Heckman, and W. Z. Rymer, “Decorrelating actions of renshaw interneurons on the firing of spinal motoneurons within a motor nucleus: a simulation study,” Journal of Neurophysiology, vol. 80, no. 1, pp. 309–323, 1998. View at Scopus
  15. F. J. Alvarez and R. E. W. Fyffe, “The continuing case for the Renshaw cell,” Journal of Physiology, vol. 584, no. 1, pp. 31–45, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  16. J. M. Tepper, C. J. Wilson, and T. Koós, “Feedforward and feedback inhibition in neostriatal GABAergic spiny neurons,” Brain Research Reviews, vol. 58, no. 2, pp. 272–281, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  17. A. Gonzalo-Ruiz and A. R. Lieberman, “GABAergic projections from the thalamic reticular nucleus to the anteroventral and anterodorsal thalamic nuclei of the rat,” Journal of Chemical Neuroanatomy, vol. 9, no. 3, pp. 165–174, 1995. View at Publisher · View at Google Scholar · View at Scopus
  18. B. J. Fredette and E. Mugnaini, “The GABAergic cerebello-olivary projection in the rat,” Anatomy and Embryology, vol. 184, no. 3, pp. 225–243, 1991. View at Scopus
  19. A. Schnitzler and J. Gross, “Normal and pathological oscillatory communication in the brain,” Nature Reviews Neuroscience, vol. 6, no. 4, pp. 285–296, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  20. T. Klausberger and P. Somogyi, “Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations,” Science, vol. 321, no. 5885, pp. 53–57, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  21. G. Birke and A. Draguhn, “No simple brake the complex functions of inhibitory synapses,” Pharmacopsychiatry, vol. 43, no. 1, pp. S21–S31, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  22. L. Wang, A. Fontanini, and A. Maffei, “Visual experience modulates spatio-temporal dynamics of circuit activation,” Frontiers in Cellular Neuroscience, vol. 5, article 12, 2011.
  23. K. Lamsa, J. H. Heeroma, and D. M. Kullmann, “Hebbian LTP in feed-forward inhibitory interneurons and the temporal fidelity of input discrimination,” Nature Neuroscience, vol. 8, no. 7, pp. 916–924, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  24. A. Semyanov, M. C. Walker, and D. M. Kullmann, “GABA uptake regulates cortical excitability via cell type-specific tonic inhibition,” Nature Neuroscience, vol. 6, no. 5, pp. 484–490, 2003. View at Scopus
  25. C. J. Wierenga and W. J. Wadman, “Miniature inhibitory postsynaptic currents in CA1 pyramidal neurons after kindling epileptogenesis,” Journal of Neurophysiology, vol. 82, no. 3, pp. 1352–1362, 1999. View at Scopus
  26. G. G. Turrigiano and S. B. Nelson, “Hebb and homeostasis in neuronal plasticity,” Current Opinion in Neurobiology, vol. 10, no. 3, pp. 358–364, 2000. View at Publisher · View at Google Scholar · View at Scopus
  27. G. G. Turrigiano and S. B. Nelson, “Homeostatic plasticity in the developing nervous system,” Nature Reviews Neuroscience, vol. 5, no. 2, pp. 97–107, 2004. View at Scopus
  28. G. G. Turrigiano, “Homeostatic plasticity in neuronal networks: the more things change, the more they stay the same,” Trends in Neurosciences, vol. 22, no. 5, pp. 221–227, 1999. View at Publisher · View at Google Scholar · View at Scopus
  29. M. Esclapez and C. R. Houser, “Up-regulation of GAD65 and GAD67 in remaining hippocampal GABA neurons in a model of temporal lobe epilepsy,” Journal of Comparative Neurology, vol. 412, no. 3, pp. 488–505, 1999. View at Publisher · View at Google Scholar · View at Scopus
  30. P. E. Garraghty, E. A. LaChica, and J. H. Kaas, “Injury-induced reorganization of somatosensory cortex is accompanied by reductions in GABA staining,” Somatosensory and Motor Research, vol. 8, no. 4, pp. 347–354, 1991. View at Scopus
  31. K. N. Hartman, S. K. Pal, J. Burrone, and V. N. Murthy, “Activity-dependent regulation of inhibitory synaptic transmission in hippocampal neurons,” Nature Neuroscience, vol. 9, no. 5, pp. 642–649, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  32. R. W. Olsen and W. Sieghart, “International Union of Pharmacology. LXX. Subtypes of γ-aminobutyric acidA receptors: classification on the basis of subunit composition, pharmacology, and function. Update,” Pharmacological Reviews, vol. 60, no. 3, pp. 243–260, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  33. J. S. Coombs, J. C. Eccles, and P. FATT, “The specific ionic conductances and the ionic movements across the motoneuronal membrane that produce the inhibitory post-synaptic potential,” The Journal of physiology, vol. 130, no. 2, pp. 326–374, 1955. View at Scopus
  34. P. Rudomin and R. F. Schmidt, “Presynaptic inhibition in the vertebrate spinal cord revisited,” Experimental Brain Research, vol. 129, no. 1, pp. 1–37, 1999. View at Publisher · View at Google Scholar · View at Scopus
  35. G. Stuart, “Voltage-activated sodium channels amplify inhibition in neocortical pyramidal neurons,” Nature Neuroscience, vol. 2, no. 2, pp. 144–150, 1999. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  36. Y. Ben-Ari, E. Cherubini, R. Corradetti, and J. L. Gaiarsa, “Giant synaptic potentials in immature rat CA3 hippocampal neurones,” Journal of Physiology, vol. 416, pp. 303–325, 1989. View at Scopus
  37. Y. Ben-Ari, J. L. Gaiarsa, R. Tyzio, and R. Khazipov, “GABA: A pioneer transmitter that excites immature neurons and generates primitive oscillations,” Physiological Reviews, vol. 87, no. 4, pp. 1215–1284, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  38. E. Cherubini, J. L. Gaiarsa, and Y. Ben-Ari, “GABA: an excitatory transmitter in early postnatal life,” Trends in Neurosciences, vol. 14, no. 12, pp. 515–519, 1991. View at Publisher · View at Google Scholar · View at Scopus
  39. R. Tyzio, C. Allene, R. Nardou et al., “Depolarizing actions of GABA in immature neurons depend neither on ketone bodies nor on pyruvate,” Journal of Neuroscience, vol. 31, no. 1, pp. 34–45, 2011. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  40. Y. Ben-Ari and G. L. Holmes, “Effects of seizures on developmental processes in the immature brain,” Lancet Neurology, vol. 5, no. 12, pp. 1055–1063, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  41. G. Huberfeld, L. Wittner, S. Clemenceau et al., “Perturbed chloride homeostasis and GABAergic signaling in human temporal lobe epilepsy,” Journal of Neuroscience, vol. 27, no. 37, pp. 9866–9873, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  42. S. Rheims, C. D. Holmgren, G. Chazal et al., “GABA action in immature neocortical neurons directly depends on the availability of ketone bodies,” Journal of Neurochemistry, vol. 110, no. 4, pp. 1330–1338, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  43. K. Kaupmann, K. Huggel, J. Heid et al., “Expression cloning of GABAB receptors uncovers similarity to metabotropic glutamate receptors,” Nature, vol. 386, no. 6622, pp. 239–246, 1997. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  44. R. Kuner, G. Kohn, S. Grunewald, G. Eisenhardt, A. Bach, and H. C. Kornau, “Role of heteromer formation in GABAB receptor function,” Science, vol. 283, no. 5398, pp. 74–77, 1999. View at Publisher · View at Google Scholar · View at Scopus
  45. N. G. Bowery and D. A. Brown, “The cloning of GABAB receptors,” Nature, vol. 386, no. 6622, pp. 223–224, 1997. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  46. U. Misgeld, M. Bijak, and W. Jarolimek, “A physiological role for GABAB receptors and the effects of baclofen in the mammalian central nervous system,” Progress in Neurobiology, vol. 46, no. 4, pp. 423–462, 1995. View at Publisher · View at Google Scholar · View at Scopus
  47. I. Mody, “Distinguishing between GABAA receptors responsible for tonic and phasic conductances,” Neurochemical Research, vol. 26, no. 8-9, pp. 907–913, 2001. View at Publisher · View at Google Scholar · View at Scopus
  48. A. Semyanov, M. C. Walker, D. M. Kullmann, and R. A. Silver, “Tonically active GABAA receptors: modulating gain and maintaining the tone,” Trends in Neurosciences, vol. 27, no. 5, pp. 262–269, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  49. N. I. Holter, M. M. Zylla, N. Zuber, C. Bruehl, and A. Draguhn, “Tonic GABAergic control of mouse dentate granule cells during postnatal development,” European Journal of Neuroscience, vol. 32, no. 8, pp. 1300–1309, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  50. M. I. Banks and R. A. Pearce, “Kinetic differences between synaptic and extrasynaptic GABAA receptors in CA1 pyramidal cells,” Journal of Neuroscience, vol. 20, no. 3, pp. 937–948, 2000. View at Scopus
  51. U. Tossman, G. Jonsson, and U. Ungerstedt, “Regional distribution and extracellular levels of amino acids in rat central nervous system,” Acta Physiologica Scandinavica, vol. 127, no. 4, pp. 533–545, 1986. View at Scopus
  52. J. Lerma, A. S. Herranz, and O. Herreras, “In vivo determination of extracellular concentration of amino acids in the rat hippocampus. A method based on brain dialysis and computerized analysis,” Brain Research, vol. 384, no. 1, pp. 145–155, 1986. View at Scopus
  53. N. Hájos, Z. Nusser, E. A. Rancz, T. F. Freund, and I. Mody, “Cell type- and synapse-specific variability in synaptic GABAA receptor occupancy,” European Journal of Neuroscience, vol. 12, no. 3, pp. 810–818, 2000. View at Publisher · View at Google Scholar · View at Scopus
  54. W. Hevers and H. Lüddens, “The diversity of GABAA receptors: pharmacological and electrophysiological properties of GABAA channel subtypes,” Molecular Neurobiology, vol. 18, no. 1, pp. 35–86, 1998. View at Scopus
  55. M. Bartos, I. Vida, M. Frotscher, J. R. P. Geiger, and P. Jonas, “Rapid signaling at inhibitory synapses in a dentate gyrus interneuron network,” Journal of Neuroscience, vol. 21, no. 8, pp. 2687–2698, 2001. View at Scopus
  56. C. J. Price, B. Cauli, E. R. Kovacs et al., “Neurogliaform neurons form a novel inhibitory network in the hippocampal CA1 area,” Journal of Neuroscience, vol. 25, no. 29, pp. 6775–6786, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  57. M. Capogna, “Neurogliaform cells and other interneurons of stratum lacunosum-moleculare gate entorhinal-hippocampal dialogue,” Journal of Physiology, vol. 589, no. 8, pp. 1875–1883, 2011. View at Publisher · View at Google Scholar · View at PubMed
  58. S. Oláh, M. Füle, G. Komlósi et al., “Regulation of cortical microcircuits by unitary GABA-mediated volume transmission,” Nature, vol. 461, no. 7268, pp. 1278–1281, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  59. S. M. Jones and M. J. Palmer, “Activation of the tonic GABAC receptor current in retinal bipolar cell terminals by nonvesicular GABA release,” Journal of Neurophysiology, vol. 102, no. 2, pp. 691–699, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  60. Y. Wu, W. Wang, A. Díez-Sampedro, and G. B. Richerson, “Nonvesicular inhibitory neurotransmission via reversal of the GABA transporter GAT-1,” Neuron, vol. 56, no. 5, pp. 851–865, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  61. A. Ströhle, E. Romeo, F. Di Michele et al., “GABAA receptor-modulating neuroactive steroid composition in patients with panic disorder before and during paroxetine treatment,” American Journal of Psychiatry, vol. 159, no. 1, pp. 145–147, 2002. View at Publisher · View at Google Scholar · View at Scopus
  62. J. Maguire and I. Mody, “Steroid hormone fluctuations and GABAAR plasticity,” Psychoneuroendocrinology, vol. 34, no. 1, pp. S84–S90, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  63. G. A. Ascoli, L. Alonso-Nanclares, S. A. Anderson et al., “Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex,” Nature Reviews Neuroscience, vol. 9, no. 7, pp. 557–568, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  64. H. Markram, M. Toledo-Rodriguez, Y. Wang, A. Gupta, G. Silberberg, and C. Wu, “Interneurons of the neocortical inhibitory system,” Nature Reviews Neuroscience, vol. 5, no. 10, pp. 793–807, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  65. P. Somogyi and T. Klausberger, “Defined types of cortical interneurone structure space and spike timing in the hippocampus,” Journal of Physiology, vol. 562, no. 1, pp. 9–26, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  66. D. Pinault, “A novel single-cell staining procedure performed in vivo under electrophysiological control: morpho-functional features of juxtacellularly labeled thalamic cells and other central neurons with biocytin or Neurobiotin,” Journal of Neuroscience Methods, vol. 65, no. 2, pp. 113–136, 1996. View at Publisher · View at Google Scholar · View at Scopus
  67. J. J. Tukker, P. Fuentealba, K. Hartwich, P. Somogyi, and T. Klausberger, “Cell type-specific tuning of hippocampal interneuron firing during gamma oscillations in vivo,” Journal of Neuroscience, vol. 27, no. 31, pp. 8184–8189, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  68. X. J. Wang and G. Buzsáki, “Gamma oscillation by synaptic inhibition in a hippocampal interneuronal network model,” Journal of Neuroscience, vol. 16, no. 20, pp. 6402–6413, 1996. View at Scopus
  69. R. D. Traub, M. O. Cunningham, T. Gloveli et al., “GABA-enhanced collective behavior in neuronal axons underlies persistent gamma-frequency oscillations,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 19, pp. 11047–11052, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  70. M. A. Whittington, R. D. Traub, N. Kopell, B. Ermentrout, and E. H. Buhl, “Inhibition-based rhythms: experimental and mathematical observations on network dynamics,” International Journal of Psychophysiology, vol. 38, no. 3, pp. 315–336, 2000. View at Publisher · View at Google Scholar · View at Scopus
  71. E. O. Mann and O. Paulsen, “Role of GABAergic inhibition in hippocampal network oscillations,” Trends in Neurosciences, vol. 30, no. 7, pp. 343–349, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  72. E. O. Mann, J. M. Suckling, N. Hajos, S. A. Greenfield, and O. Paulsen, “Perisomatic feedback inhibition underlies cholinergically induced fast network oscillations in the rat hippocampus in vitro,” Neuron, vol. 45, no. 1, pp. 105–117, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  73. S. K. Towers, F. E. N. LeBeau, T. Gloveli, R. D. Traub, M. A. Whittington, and E. H. Buhl, “Fast network oscillations in the rat dentate gyrus in vitro,” Journal of Neurophysiology, vol. 87, no. 2, pp. 1165–1168, 2002. View at Scopus
  74. M. Blatow, A. Rozov, I. Katona et al., “A novel network of multipolar bursting interneurons generates theta frequency oscillations in neocortex,” Neuron, vol. 38, no. 5, pp. 805–817, 2003. View at Publisher · View at Google Scholar · View at Scopus
  75. M. Bartos, I. Vida, M. Frotscher et al., “Fast synaptic inhibition promotes synchronized gamma oscillations in hippocampal interneuron networks,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 20, pp. 13222–13227, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  76. S. R. Cobb, E. H. Buhl, K. Halasy, O. Paulsen, and P. Somogyl, “Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons,” Nature, vol. 378, no. 6552, pp. 75–78, 1995. View at Scopus
  77. E. A. Barnard, P. Skolnick, R. W. Olsen et al., “International union of pharmacology. XV. Subtypes of γ-aminobutyric acidA receptors: classification on the basis of subunit structure and receptor function,” Pharmacological Reviews, vol. 50, no. 2, pp. 291–313, 1998. View at Scopus
  78. A. K. Mehta and M. K. Ticku, “An update on GABAA receptors,” Brain Research Reviews, vol. 29, no. 2-3, pp. 196–217, 1999. View at Publisher · View at Google Scholar · View at Scopus
  79. I. Mody and R. A. Pearce, “Diversity of inhibitory neurotransmission through GABAA receptors,” Trends in Neurosciences, vol. 27, no. 9, pp. 569–575, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  80. C. Essrich, M. Lorez, J. A. Benson, J. M. Fritschy, and B. Lüscher, “Postsynaptic clustering of major GABAA receptor subtypes requires the γ2 subunit and gephyrin,” Nature Neuroscience, vol. 1, no. 7, pp. 563–571, 1998. View at Scopus
  81. J. T. Kittler, K. McAinsh, and S. J. Moss, “Mechanisms of GABAA receptor assembly and trafficking: implications for the modulation of inhibitory neurotransmission,” Molecular Neurobiology, vol. 26, no. 2-3, pp. 251–268, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  82. M. Giustetto, J. Kirsch, J. M. Fritschy, D. Cantino, and M. Sassoè-Pognetto, “Localization of the clustering protein gephyrin at GABAergic synapses in the main olfactory bulb of the rat,” Journal of Comparative Neurology, vol. 395, no. 2, pp. 231–244, 1998. View at Publisher · View at Google Scholar · View at Scopus
  83. M. Kneussel and H. Betz, “Clustering of inhibitory neurotransmitter receptors at developing postsynaptic sites: the membrane activation model,” Trends in Neurosciences, vol. 23, no. 9, pp. 429–435, 2000. View at Publisher · View at Google Scholar · View at Scopus
  84. J. W. Mozrzymas, E. D. Zarmowska, M. Pytel, and K. Mercik, “Modulation of GABAA receptors by hydrogen ions reveals synaptic GABA transient and a crucial role of the desensitization process,” Journal of Neuroscience, vol. 23, no. 22, pp. 7981–7992, 2003. View at Scopus
  85. A. Barberis, E. M. Petrini, and E. Cherubini, “Presynaptic source of quantal size variability at GABAergic synapses in rat hippocampal neurons in culture,” European Journal of Neuroscience, vol. 20, no. 7, pp. 1803–1810, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  86. J. Glykys and I. Mody, “The main source of ambient GABA responsible for tonic inhibition in the mouse hippocampus,” Journal of Physiology, vol. 582, no. 3, pp. 1163–1178, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  87. J. C. Eccles, R. F. Schmidt, and W. D. Willis, “Presynaptic inhibition of the spinal monosynaptic reflex pathway,” The Journal of physiology, vol. 161, pp. 282–297, 1962. View at Scopus
  88. H. Alle and J. R. P. Geiger, “GABAergic spill-over transmission onto hippocampal mossy fiber boutons,” Journal of Neuroscience, vol. 27, no. 4, pp. 942–950, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  89. S. F. Stasheff, D. D. Mott, and W. A. Wilson, “Axon terminal hyperexcitability associated with epileptogenesis in vitro. II. Pharmacological regulation by NMDA and GABAA receptors,” Journal of Neurophysiology, vol. 70, no. 3, pp. 976–984, 1993. View at Scopus
  90. B. M. Stell, P. Rostaing, A. Triller, and A. Marty, “Activation of presynaptic GABAA receptors induces glutamate release from parallel fiber synapses,” Journal of Neuroscience, vol. 27, no. 34, pp. 9022–9031, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  91. S. L. Hansen, B. Fjalland, and M. B. Jackson, “Modulation of GABAA receptors and neuropeptide secretion by the neurosteroid allopregnanolone in posterior and intermediate pituitary,” Pharmacology and Toxicology, vol. 93, no. 2, pp. 91–97, 2003. View at Publisher · View at Google Scholar
  92. A. Draguhn, N. Axmacher, and S. Kolbaev, “Presynaptic ionotropic GABA receptors,” Results and Problems in Cell Differentiation, vol. 44, pp. 69–85, 2007. View at Publisher · View at Google Scholar · View at PubMed
  93. D. M. Kullmann, “Spillover and synaptic cross talk mediated by glutamate and GABA in the mammalian brain,” Progress in Brain Research, vol. 125, pp. 339–351, 2000. View at Publisher · View at Google Scholar · View at Scopus
  94. M. Scanziani, “GABA spillover activates postsynaptic GABAB receptors to control rhythmic hippocampal activity,” Neuron, vol. 25, no. 3, pp. 673–681, 2000. View at Scopus
  95. K. E. Vogt and R. A. Nicoll, “Glutamate and γ-aminobutyric acid mediate a heterosynaptic depression at mossy fiber synapses in the hippocampus,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 3, pp. 1118–1122, 1999. View at Publisher · View at Google Scholar · View at Scopus
  96. J. S. Isaacson, J. M. Solis, and R. A. Nicoll, “Local and diffuse synaptic actions of GABA in the hippocampus,” Neuron, vol. 10, no. 2, pp. 165–175, 1993. View at Publisher · View at Google Scholar · View at Scopus
  97. Y. Wang, F. B. Neubauer, H. R. Lüscher, and K. Thurley, “GABAB receptor-dependent modulation of network activity in the rat prefrontal cortex in vitro,” European Journal of Neuroscience, vol. 31, no. 9, pp. 1582–1594, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  98. J. N. Cammack, S. V. Rakhilin, and E. A. Schwartz, “A GABA transporter operates asymmetrically and with variable stoichiometry,” Neuron, vol. 13, no. 4, pp. 949–960, 1994. View at Publisher · View at Google Scholar · View at Scopus
  99. J. L. Corey, J. Guastella, N. Davidson, and H. A. Lester, “GABA uptake and release by a mammalian cell line stably expressing a cloned rat brain GABA transporter,” Molecular membrane biology, vol. 11, no. 1, pp. 23–30, 1994. View at Scopus
  100. D. Attwell, B. Barbour, and M. Szatkowski, “Nonvesicular release of neurotransmitter,” Neuron, vol. 11, no. 3, pp. 401–407, 1993. View at Publisher · View at Google Scholar · View at Scopus
  101. M. J. During, K. M. Ryder, and D. D. Spencer, “Hippocampal GABA transporter function in temporal-lobe epilepsy,” Nature, vol. 376, no. 6536, pp. 174–177, 1995. View at Scopus
  102. A. Yamauchi, S. Uchida, H. M. Kwon et al., “Cloning of a Na+- and Cl--dependent betaine transporter that is regulated by hypertonicity,” Journal of Biological Chemistry, vol. 267, no. 1, pp. 649–652, 1992. View at Scopus
  103. J. Guastella, N. Nelson, H. Nelson et al., “Cloning and expression of a rat brain GABA transporter,” Science, vol. 249, no. 4974, pp. 1303–1306, 1990. View at Scopus
  104. B. I. Kanner and A. Bendahan, “Two pharmacologically distinct sodium- and chloride-coupled high-affinity γ-aminobutyric acid transporters are present in plasma membrane vesicles and reconstituted preparations from rat brain,” Proceedings of the National Academy of Sciences of the United States of America, vol. 87, no. 7, pp. 2550–2554, 1990. View at Scopus
  105. Q. -R. Liu, B. Lopez-Corcuera, S. Mandiyan, H. Nelson, and N. Nelson, “Molecular characterization of four pharmacologically distinct gamma-aminobutyric acid transporters in mouse brain,” Journal of Biological Chemistry, vol. 268, no. 3, pp. 2106–2112, 1993.
  106. L. A. Borden, K. E. Smith, P. R. Hartig, T. A. Branchek, and R. L. Weinshank, “Molecular heterogeneity of the γ-aminobutyric acid (GABA) transport system. Cloning of two novel high affinity GABA transporters from rat brain,” Journal of Biological Chemistry, vol. 267, no. 29, pp. 21098–21104, 1992. View at Scopus
  107. A. Schousboe and H. S. Waagepetersen, “GABA: homeostatic and pharmacological aspects,” Progress in Brain Research, vol. 160, pp. 9–19, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  108. F. Conti, M. Melone, S. De Biasi, A. Minelli, N. C. Brecha, and A. Ducati, “Neuronal and glial localization of GAT-1, a high-affinity γ-aminobutyric acid plasma membrane transporter, in human cerebral cortex: with a note on its distribution in monkey cortex,” Journal of Comparative Neurology, vol. 396, no. 1, pp. 51–63, 1998. View at Publisher · View at Google Scholar
  109. A. Minelli, S. DeBiasi, N. C. Brecha, L. V. Zuccarello, and F. Conti, “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,” Journal of Neuroscience, vol. 16, no. 19, pp. 6255–6264, 1996. View at Scopus
  110. C. E. Ribak, W. M. Y. Tong, and N. C. Brecha, “GABA plasma membrane transporters, GAT-1 and GAT-3, display different distributions in the rat hippocampus,” Journal of Comparative Neurology, vol. 367, no. 4, pp. 595–606, 1996. View at Publisher · View at Google Scholar · View at Scopus
  111. J. D. Rothstein, L. Martin, A. I. Levey et al., “Localization of neuronal and glial glutamate transporters,” Neuron, vol. 13, no. 3, pp. 713–725, 1994. View at Publisher · View at Google Scholar · View at Scopus
  112. F. Conti, S. DeBiasi, A. Minelli, J. D. Rothstein, and M. Melone, “EAAC1, a high-affinity glutamate transporter, is localized to astrocytes and gabaergic neurons besides pyramidal cells in the rat cerebral cortex,” Cerebral Cortex, vol. 8, no. 2, pp. 108–116, 1998. View at Publisher · View at Google Scholar
  113. Y. He, W. G. M. Janssen, J. D. Rothstein, and J. H. Morrison, “Differential synaptic localization of the glutamate transporter EAAC1 and glutamate receptor subunit GluR2 in the rat hippocampus,” Journal of Comparative Neurology, vol. 418, no. 3, pp. 255–269, 2000. View at Publisher · View at Google Scholar · View at Scopus
  114. O. M. Larsson, J. Drejer, E. Kvamme, G. Svenneby, L. Hertz, and A. Schousboe, “Ontogenetic development of glutamate and GABA metabolizing enzymes in cultured cerebral cortex interneurons and in cerebral cortex in vivo,” International Journal of Developmental Neuroscience, vol. 3, no. 2, pp. 177–185, 1985. View at Scopus
  115. M. Melone, F. Quagliano, P. Barbaresi, H. Varoqui, J. D. Erickson, and F. Conti, “Localization of the glutamine transporter SNAT1 in rat cerebral cortex and neighboring structures, with a note on its localization in human cortex,” Cerebral Cortex, vol. 14, no. 5, pp. 562–574, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  116. M. G. Erlander and A. J. Tobin, “The structural and functional heterogeneity of glutamic acid decarboxylase: a review,” Neurochemical Research, vol. 16, no. 3, pp. 215–226, 1991. View at Scopus
  117. M. Esclapez, N. J. K. Tillakaratne, D. L. Kaufman, A. J. Tobin, and C. R. Houser, “Comparative localization of two forms of glutamic acid decarboxylase and their mRNAs in rat brain supports the concept of functional differences between the forms,” Journal of Neuroscience, vol. 14, no. 3, pp. 1834–1855, 1994. View at Scopus
  118. H. Jin, H. Wu, G. Osterhaus et al., “Demonstration of functional coupling between γ-aminobutyric acid (GABA) synthesis and vesicular GABA transport into synaptic vesicles,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 7, pp. 4293–4298, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  119. I. Jacobson, M. Sandberg, and A. Hamberger, “Mass transfer in brain dialysis devices—a new method for the estimation of extracellular amino acids concentration,” Journal of Neuroscience Methods, vol. 15, no. 3, pp. 263–268, 1985. View at Scopus
  120. K. Kanamori and B. D. Ross, “Quantitative determination of extracellular glutamine concentration in rat brain, and its elevation in vivo by system A transport inhibitor, α-(methylamino)isobutyrate,” Journal of Neurochemistry, vol. 90, no. 1, pp. 203–210, 2004. View at Publisher · View at Google Scholar · View at PubMed
  121. L. K. Bak, A. Schousboe, and H. S. Waagepetersen, “The glutamate/GABA-glutamine cycle: aspects of transport, neurotransmitter homeostasis and ammonia transfer,” Journal of Neurochemistry, vol. 98, no. 3, pp. 641–653, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  122. S. Bröer and N. Brookes, “Transfer of glutamine between astrocytes and neurons,” Journal of Neurochemistry, vol. 77, no. 3, pp. 705–719, 2001. View at Publisher · View at Google Scholar · View at Scopus
  123. I. M. González-González, B. Cubelos, C. Giménez, and F. Zafra, “Immunohistochemical localization of the amino acid transporter SNAT2 in the rat brain,” Neuroscience, vol. 130, no. 1, pp. 61–73, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  124. S. L. Liang, G. C. Carlson, and D. A. Coulter, “Dynamic regulation of synaptic GABA release by the glutamate-glutamine cycle in hippocampal area CA1,” Journal of Neuroscience, vol. 26, no. 33, pp. 8537–8548, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  125. M. N. Fricke, D. M. Jones-Davis, and G. C. Mathews, “Glutamine uptake by System A transporters maintains neurotransmitter GABA synthesis and inhibitory synaptic transmission,” Journal of Neurochemistry, vol. 102, no. 6, pp. 1895–1904, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  126. A. S. Bryant, B. Li, M. P. Beenhakker, and J. R. Huguenard, “Maintenance of thalamic epileptiform activity depends on the astrocytic glutamate-glutamine cycle,” Journal of Neurophysiology, vol. 102, no. 5, pp. 2880–2888, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  127. H. Tani, A. E. Bandrowski, I. Parada et al., “Modulation of epileptiform activity by glutamine and System A transport in a model of post-traumatic epilepsy,” Neurobiology of Disease, vol. 25, no. 2, pp. 230–238, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  128. M. N. Brown and G. C. Mathews, “Activity- and age-dependent modulation of GABAergic neurotransmission by System A-mediated glutamine uptake,” Journal of Neurochemistry, vol. 114, no. 3, pp. 909–920, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  129. G. Ahnert-Hilger and R. Jahn, “CLC-3 spices up GABAergic synaptic vesicles,” Nature Neuroscience, vol. 14, no. 4, pp. 405–407, 2011. View at Publisher · View at Google Scholar · View at PubMed
  130. C. C. Hsu, C. Thomas, W. Chen et al., “Role of synaptic vesicle proton gradient and protein phosphorylation on ATP-mediated activation of membrane-associated brain glutamate decarboxylase,” Journal of Biological Chemistry, vol. 274, no. 34, pp. 24366–24371, 1999. View at Publisher · View at Google Scholar · View at Scopus
  131. V. Riazanski, L. V. Deriy, P. D. Shevchenko, B. Le, E. A. Gomez, and D. J. Nelson, “Presynaptic CLC-3 determines quantal size of inhibitory transmission in the hippocampus,” Nature Neuroscience, vol. 14, no. 4, pp. 487–494, 2011. View at Publisher · View at Google Scholar · View at PubMed
  132. J. D. Erickson, S. De Gois, H. Varoqui, M. K. H. Schafer, and E. Weihe, “Activity-dependent regulation of vesicular glutamate and GABA transporters: a means to scale quantal size,” Neurochemistry International, vol. 48, no. 6-7, pp. 643–649, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  133. J. W. Hell, L. Edelmann, J. Hartinger, and R. Jahn, “Functional reconstitution of the γ-aminobutyric acid transporter from synaptic vesicles using artificial ion gradients,” Biochemistry, vol. 30, no. 51, pp. 11795–11800, 1991. View at Scopus
  134. P. Jonas, J. Bischofberger, and J. Sandkühler, “Corelease of two fast neurotransmitters at a central synapse,” Science, vol. 281, no. 5375, pp. 419–424, 1998. View at Publisher · View at Google Scholar · View at Scopus
  135. R. H. Edwards, “The neurotransmitter cycle and quantal size,” Neuron, vol. 55, no. 6, pp. 835–858, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  136. S. Takamori, M. Holt, K. Stenius et al., “Molecular anatomy of a trafficking organelle,” Cell, vol. 127, no. 4, pp. 831–846, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  137. J. Williams, “How does a vesicle know it is full?” Neuron, vol. 18, no. 5, pp. 683–686, 1997. View at Publisher · View at Google Scholar · View at Scopus
  138. M. J. Jung, B. Lippert, and B. W. Metcalf, “The effect of 4 amino hex 5 ynoic acid (γ acetylenic GABA, γ ethynyl GABA) a catalytic inhibitor of GABA transaminase, on brain GABA metabolism in vivo,” Journal of Neurochemistry, vol. 28, no. 4, pp. 717–723, 1977.
  139. I. Schousboe, B. Bro, and A. Schousboe, “Intramitochondrial localization of the 4 aminobutyrate 2 oxoglutarate transaminase from ox brain,” Biochemical Journal, vol. 162, no. 2, pp. 303–307, 1977. View at Scopus
  140. P. Kugler, “In situ measurements of enzyme activities in the brain,” Histochemical Journal, vol. 25, no. 5, pp. 329–338, 1993. View at Publisher · View at Google Scholar · View at Scopus
  141. J. A. Eckstein, G. M. Ammerman, J. M. Reveles, and B. L. Ackermann, “Analysis of glutamine, glutamate, pyroglutamate, and GABA in cerebrospinal fluid using ion pairing HPLC with positive electrospray LC/MS/MS,” Journal of Neuroscience Methods, vol. 171, no. 2, pp. 190–196, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  142. P. M. Burger, E. Mehl, P. L. Cameron et al., “Synaptic vesicles immunoisolated from rat cerebral cortex contain high levels of glutamate,” Neuron, vol. 3, no. 6, pp. 715–720, 1989. View at Scopus
  143. A. Barberis, E. M. Petrini, and J. W. Mozrzymas, “Impact of synaptic neurotransmitter concentration time course on the kinetics and pharmacological modulation of inhibitory synaptic currents,” Frontiers in Cellular Neuroscience, vol. 5, article 6, 2011.
  144. J. W. Mozrzymas, A. Barberis, K. Michalak, and E. Cherubini, “Chlorpromazine inhibits miniature GABAergic currents by reducing the binding and by increasing the unbinding rate of GABAA receptors,” Journal of Neuroscience, vol. 19, no. 7, pp. 2474–2488, 1999. View at Scopus
  145. M. V. Jones and G. L. Westbrook, “Desensitized states prolong GABAA channel responses to brief agonist pulses,” Neuron, vol. 15, no. 1, pp. 181–191, 1995. View at Scopus
  146. D. J. Maconochie, J. M. Zempel, and J. H. Steinbach, “How quickly can GABAA receptors open?” Neuron, vol. 12, no. 1, pp. 61–71, 1994. View at Scopus
  147. D. Perrais and N. Ropert, “Effect of zolpidem on miniature IPSCs and occupancy of postsynaptic GABAA receptors in central synapses,” Journal of Neuroscience, vol. 19, no. 2, pp. 578–588, 1999. View at Scopus
  148. G. Buzsáki, D. L. Buhl, K. D. Harris, J. Csicsvari, B. Czéh, and A. Morozov, “Hippocampal network patterns of activity in the mouse,” Neuroscience, vol. 116, no. 1, pp. 201–211, 2003. View at Publisher · View at Google Scholar · View at Scopus
  149. H. Berger, “Über das Elektrenkephalogramm des Menschen,” Archiv für Psychiatrie und Nervenkrankheiten, vol. 87, no. 1, pp. 527–570, 1929. View at Publisher · View at Google Scholar · View at Scopus
  150. J. Csicsvari, H. Hirase, A. Czurkó, A. Mamiya, and G. Buzsáki, “Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving rat,” Journal of Neuroscience, vol. 19, no. 1, pp. 274–287, 1999. View at Scopus
  151. F. Bähner, E. K. Weiss, G. Birke et al., “Cellular correlate of assembly formation in oscillating hippocampal networks in vitro,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 35, pp. E607–E616, 2011. View at Publisher · View at Google Scholar · View at PubMed
  152. L. A. Tremere and R. Pinaud, “Incongruent restoration of inhibitory transmission and general metabolic activity during reorganization of somatosensory cortex,” International Journal of Neuroscience, vol. 115, no. 7, pp. 1003–1015, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  153. M. Costa-Mattioli, W. S. Sossin, E. Klann, and N. Sonenberg, “Translational control of long-lasting synaptic plasticity and memory,” Neuron, vol. 61, no. 1, pp. 10–26, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  154. Y. Lu, K. Christian, and B. Lu, “BDNF: a key regulator for protein synthesis-dependent LTP and long-term memory?” Neurobiology of Learning and Memory, vol. 89, no. 3, pp. 312–323, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  155. C. P. Bengtson, H. E. Freitag, J. M. Weislogel, and H. Bading, “Nuclear calcium sensors reveal that repetition of trains of synaptic stimuli boosts nuclear calcium signaling in CA1 pyramidal neurons,” Biophysical Journal, vol. 99, no. 12, pp. 4066–4077, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  156. J. M. Frade and Y. A. Barde, “Nerve growth factor: two receptors, multiple functions,” BioEssays, vol. 20, no. 2, pp. 137–145, 1998. View at Publisher · View at Google Scholar · View at Scopus
  157. R. Gutiérrez, “The dual glutamatergic-GABAergic phenotype of hippocampal granule cells,” Trends in Neurosciences, vol. 28, no. 6, pp. 297–303, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  158. G. Gómez-Lira, M. Lamas, H. Romo-Parra, and R. Gutiérrez, “Programmed and induced phenotype of the hippocampal granule cells,” Journal of Neuroscience, vol. 25, no. 30, pp. 6939–6946, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  159. M. C. Walker, A. Ruiz, and D. M. Kullmann, “Do mossy fibers release GABA?” Epilepsia, vol. 43, no. 5, pp. 196–202, 2002. View at Publisher · View at Google Scholar · View at Scopus
  160. J. R. Gomes, A. C. Lobo, C. V. Melo et al., “Cleavage of the vesicular GABA transporter under excitotoxic conditions is followed by accumulation of the truncated transporter in nonsynaptic sites,” Journal of Neuroscience, vol. 31, no. 12, pp. 4622–4635, 2011. View at Publisher · View at Google Scholar · View at PubMed
  161. M. Lamas, G. Gómez-Lira, and R. Gutiérrez, “Vesicular GABA transporter mRNA expression in the dentate gyrus and in mossy fiber synaptosomes,” Molecular Brain Research, vol. 93, no. 2, pp. 209–214, 2001. View at Publisher · View at Google Scholar · View at Scopus
  162. J. P. Sepkuty, A. S. Cohen, C. Eccles et al., “A neuronal glutamate transporter contributes to neurotransmitter GABA synthesis and epilepsy,” Journal of Neuroscience, vol. 22, no. 15, pp. 6372–6379, 2002. View at Scopus
  163. B. Hinz, A. Becher, D. Mitter et al., “Activity-dependent changes of the presynaptic synaptophysin-synaptobrevin complex in adult rat brain,” European Journal of Cell Biology, vol. 80, no. 10, pp. 615–619, 2001. View at Scopus
  164. G. C. Mathews and J. S. Diamond, “Neuronal glutamate uptake contributes to GABA synthesis and inhibitory synaptic strength,” Journal of Neuroscience, vol. 23, no. 6, pp. 2040–2048, 2003. View at Scopus
  165. K. Hartmann, C. Bruehl, T. Golovko, and A. Draguhn, “Fast homeostatic plasticity of inhibition via activity-dependent vesicular filling,” PLoS One, vol. 3, no. 8, Article ID e2979, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  166. K. Kirmse, A. Dvorzhak, S. Kirischuk, and R. Grantyn, “GABA transporter 1 tunes GABAergic synaptic transmission at output neurons of the mouse neostriatum,” Journal of Physiology, vol. 586, no. 23, pp. 5665–5678, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  167. A. Draguhn and U. Heinemann, “Different mechanisms regulate IPSC kinetics in early postnatal and juvenile hippocampal granule cells,” Journal of Neurophysiology, vol. 76, no. 6, pp. 3983–3993, 1996. View at Scopus
  168. S. Krause and W. Schwarz, “Identification and selective inhibition of the channel mode of the neuronal GABA transporter 1,” Molecular Pharmacology, vol. 68, no. 6, pp. 1728–1735, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  169. L. Gram, O. M. Larsson, A. H. Johnsen, and A. Schousboe, “Effects of valproate, vigabatrin and aminooxyacetic acid on release of endogenous and exogenous GABA from cultured neurons,” Epilepsy Research, vol. 2, no. 2, pp. 87–95, 1988. View at Scopus
  170. W. Loscher, R. Jackel, and F. Muller, “Anticonvulsant and proconvulsant effects of inhibitors of GABA degradation in the amygdala-kindling model,” European Journal of Pharmacology, vol. 163, no. 1, pp. 1–14, 1989. View at Scopus
  171. M. Bialer, S. I. Johannessen, H. J. Kupferberg, R. H. Levy, P. Loiseau, and E. Perucca, “Progress report on new antiepileptic drugs: a summary of The Fourth Eilat Conference (EILAT IV),” Epilepsy Research, vol. 34, no. 1, pp. 1–41, 1999. View at Publisher · View at Google Scholar · View at Scopus
  172. J. A. Cramer, R. Fisher, E. Ben-Menachem, J. French, and R. H. Mattson, “New antiepileptic drugs: comparison of key clinical trials,” Epilepsia, vol. 40, no. 5, pp. 590–600, 1999. View at Scopus
  173. D. Engel, I. Pahner, K. Schulze et al., “Plasticity of rat central inhibitory synapses through GABA metabolism,” Journal of Physiology, vol. 535, no. 2, pp. 473–482, 2001. View at Publisher · View at Google Scholar · View at Scopus
  174. N. Axmacher and A. Draguhn, “Inhibition of GABA release by presynaptic ionotropic GABA receptors in hippocampal CA3,” NeuroReport, vol. 15, no. 2, pp. 329–334, 2004. View at Publisher · View at Google Scholar · View at Scopus
  175. W. H. Butler, G. P. Ford, and J. W. Newberne, “A study of the effects of vigabatrin on the central nervous system and retina of Sprague Dawley and Lister-Hooded rats,” Toxicologic Pathology, vol. 15, no. 2, pp. 143–148, 1987.
  176. A. Schousboe, G. Svenneby, and L. Hertz, “Uptake and metabolism of glutamate in astrocytes cultured from dissociated mouse brain hemispheres,” Journal of Neurochemistry, vol. 29, no. 6, pp. 999–1005, 1977. View at Scopus