Activity-dependent plasticity of astroglial potassium and glutamate clearance

Neural Plasticity

Volumn 2015, Issue , 2015, Pages

  Cheung, Giselle ^a   Sibille, Jérémie ^a,b   Zapata, Jonathan ^a   Rouach, Nathalie ^a  

^a PSL RESEARCH UNIVERSITY   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTAMATE TRANSPORTER; GLUTAMIC ACID; POTASSIUM CHANNEL; POTASSIUM ION; POTASSIUM; VESICULAR GLUTAMATE TRANSPORTER;

ASTROCYTE; BRAIN FUNCTION; CLEARANCE; ELECTROPHYSIOLOGICAL PROCEDURES; EXCITATORY POSTSYNAPTIC POTENTIAL; EXTRACELLULAR SPACE; GAP JUNCTION; HUMAN; MOLECULAR DYNAMICS; NERVE CELL EXCITABILITY; NERVE CELL PLASTICITY; NERVE CELL STIMULATION; NEUROTRANSMISSION; NONHUMAN; POTASSIUM CURRENT; REGULATORY MECHANISM; REVIEW; SYNAPTIC TRANSMISSION; ANIMAL; METABOLISM; PHYSIOLOGY;

ANIMALS; ASTROCYTES; GLUTAMIC ACID; HUMANS; NEURONAL PLASTICITY; POTASSIUM; VESICULAR GLUTAMATE TRANSPORT PROTEINS;

EID: 84939628586     PISSN: 20905904     EISSN: 16875443     Source Type: Journal    
DOI: 10.1155/2015/109106     Document Type: Review

References (124)

1. J. A. Orellana, P. J. Sáez, C. Cortés-campos et al., "Glucose increases intracellular free Ca2+ in tanycytes via ATP released through connexin 43 hemichannels, " Glia, vol. 60, no. 1, pp. 53-68, 2012.
2. N. Rouach, E. Avignone, W. Même et al., "Gap junctions and connexin expression in the normal and pathological central nervous system, " Biology of the Cell, vol. 94, no. 7-8, pp. 457-475, 2002.
3. M. V. Sofroniew and H. V. Vinters, "Astrocytes: biology and pathology, " Acta Neuropathologica, vol. 119, no. 1, pp. 7-35, 2010.
4. G. Dallérac, O. Chever, and N. Rouach, "How do astrocytes shape synaptic transmission? Insights from electrophysiology, " Frontiers in Cellular Neuroscience, vol. 7, article 159, 2013.
5. Y. Ota, A. T. Zanetti, and R.M. Hallock, "The role of astrocytes in the regulation of synaptic plasticity and memory formation, " Neural Plasticity, vol. 2013, Article ID 185463, 11 pages, 2013.
6. U. Pannasch, L. Vargová, J. Reingruber et al., "Astroglial networks scale synaptic activity and plasticity, " Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 20, pp. 8467-8472, 2011.
7. G. Perea, M. Navarrete, and A. Araque, "Tripartite synapses: astrocytes process and control synaptic information, " Trends in Neurosciences, vol. 32, no. 8, pp. 421-431, 2009.
8. A. Volterra and J. Meldolesi, "Astrocytes, from brain glue to communication elements: the revolution continues, " Nature Reviews Neuroscience, vol. 6, no. 8, pp. 626-640, 2005.
9. U. Pannasch and N. Rouach, "Emerging role for astroglial networks in information processing: from synapse to behavior, " Trends in Neurosciences, vol. 36, no. 7, pp. 405-417, 2013.
10. T. C. Bellamy and D. Ogden, "Short-term plasticity of Bergmann glial cell extrasynaptic currents during parallel fiber stimulation in rat cerebellum, " Glia, vol. 52, no. 4, pp. 325-335, 2005.
11. T. C. Bellamy and D. Ogden, "Long-term depression of neuron to glial signalling in rat cerebellar cortex, " European Journal of Neuroscience, vol. 23, no. 2, pp. 581-586, 2006.
12. J. S. Diamond, D. E. Bergles, and C. E. Jahr, "Glutamate release monitored with astrocyte transporter currents during LTP, " Neuron, vol. 21, no. 2, pp. 425-433, 1998.
13. W.-P. Ge and S. Duan, "Persistent enhancement of neuron-glia signaling mediated by increased extracellular K+ accompanying long-term synaptic potentiation, " Journal of Neurophysiology, vol. 97, no. 3, pp. 2564-2569, 2007.
14. C. Genoud, C. Quairiaux, P. Steiner, H. Hirling, E. Welker, and G. W. Knott, "Plasticity of astrocytic coverage and glutamate transporter expression in adult mouse cortex, " PLoS Biology, vol. 4, no. 11, article e343, 2006.
15. D. J. Linden, "Long-term potentiation of glial synaptic currents in cerebellar culture, " Neuron, vol. 18, no. 6, pp. 983-994, 1997.
16. D. J. Linden, "Synaptically evoked glutamate transport currents may be used to detect the expression of long-term potentiation in cerebellar culture, " Journal of Neurophysiology, vol. 79, no. 6, pp. 3151-3156, 1998.
17. S. H. R. Oliet, R. Piet, and D. A. Poulain, "Control of glutamate clearance and synaptic efficacy by glial coverage of neurons, " Science, vol. 292, no. 5518, pp. 923-926, 2001.
18. U. Pannasch, D. Freche, G. Dallérac et al., "Connexin 30 sets synaptic strength by controlling astroglial synapse invasion, " Nature Neuroscience, vol. 17, no. 4, pp. 549-558, 2014.
19. J.D. Pita-Almenar, M. S. Collado, C. M. Colbert, and A. Eskin, "Different mechanisms exist for the plasticity of glutamate reuptake during early long-term potentiation (LTP) and late LTP, " Journal of Neuroscience, vol. 26, no. 41, pp. 10461-10471, 2006.
20. J. D. Pita-Almenar, S. Zou, C. M. Colbert, and A. Eskin, "Relationship between increase in astrocytic GLT-1 glutamate transport and late-LTP, " Learning and Memory, vol. 19, no. 12, pp. 615-626, 2012.
21. J. Sibille, U. Pannasch, and N. Rouach, "Astroglial potassium clearance contributes to short-term plasticity of synaptically evoked currents at the tripartite synapse, " The Journal of Physiology, vol. 592, no. 1, pp. 87-102, 2014.
22. X. Zhang, J. Zhang, and C. Chen, "Long-term potentiation at hippocampal perforant path-dentate astrocyte synapses, " Biochemical and Biophysical Research Communications, vol. 383, no. 3, pp. 326-330, 2009.
23. N. P. Poolos, M. D. Mauk, and J. D. Kocsis, "Activity-evoked increases in extracellular potassium modulate presynaptic excitability in the CA1 region of the hippocampus, " Journal of Neurophysiology, vol. 58, no. 2, pp. 404-416, 1987.
24. W. J. Adelman Jr. and R. Fitzhugh, "Solutions of the Hodgkin Huxley equations modified for potassium accumulation in a periaxonal space, " Federation Proceedings, vol. 34, no. 5, pp. 1322-1329, 1975.
25. U. Heinemann and H.D. Lux, "Ceiling of stimulus induced rises in extracellular potassium concentration in the cerebral cortex of cat, " Brain Research, vol. 120, no. 2, pp. 231-249, 1977.
26. W. Walz, "Role of astrocytes in the clearance of excess extracellular potassium, " Neurochemistry International, vol. 36, no. 4-5, pp. 291-300, 2000.
27. N. C. Danbolt, "Glutamate uptake, " Progress in Neurobiology, vol. 65, no. 1, pp. 1-105, 2001.
28. N. Riveros, J. Fiedler, N. Lagos, C. Muñoz, and F. Orrego, "Glutamate in rat brain cortex synaptic vesicles: influence of the vesicle isolation procedure, " Brain Research, vol. 386, no. 1-2, pp. 405-408, 1986.
29. J. A. Dzubay and C. E. Jahr, "The concentration of synaptically released glutamate outside of the climbing fiber-Purkinje cell synaptic cleft, " The Journal of Neuroscience, vol. 19, no. 13, pp. 5265-5274, 1999.
30. V. I. Chefer, A. C. Thompson, A. Zapata, and T. S. Shippenberg, "Overview of brain microdialysis, " Current Protocols in Neuroscience, chapter 7: unit 7.1, 2009.
31. M. A. Herman and C. E. Jahr, "Extracellular glutamate concentration in hippocampal slice, " Journal of Neuroscience, vol. 27, no. 36, pp. 9736-9741, 2007.
32. K. Moussawi, A. Riegel, S. Nair, and P.W. Kalivas, "Extracellular glutamate: functional compartments operate in different concentration ranges, " Frontiers in Systems Neuroscience, no. 2011, article 94, 2011.
33. P. Kofuji and E. A. Newman, "Potassium buffering in the central nervous system, " Neuroscience, vol. 129, no. 4, pp. 1045-1056, 2004.
34. A. R. G. Medwin, "A study of the mechanisms by which potassium moves through brain tissue in the rat, " The Journal of Physiology, vol. 335, pp. 353-374, 1983.
35. B. R. Ransom, "Do glial gap junctions play a role in extracellular ion homeostasis?" in Gap Junctions in the Nervous System, D. C. Spray and R. Dermietzel, Eds., pp. 159-173, RG Landes Company, Austin, Tex, USA, 1996.
36. H. Hibino, A. Inanobe, K. Furutani, S. Murakami, I. Findlay, and Y. Kurachi, "Inwardly rectifying potassium channels: their structure, function, and physiological roles, " Physiological Reviews, vol. 90, no. 1, pp. 291-366, 2010.
37. C. G. Nichols and A. N. Lopatin, "Inward rectifier potassium channels, " Annual Review of Physiology, vol. 59, pp. 171-191, 1997.
38. H. Sontheimer, "Voltage-dependent ion channels in glial cells, " Glia, vol. 11, no. 2, pp. 156-172, 1994.
39. T. Takumi, T. Ishii, Y. Horio et al., "A novel ATP-dependent inward rectifier potassium channel expressed predominantly in glial cells, " Journal of Biological Chemistry, vol. 270, no. 27, pp. 16339-16346, 1995.
40. K. Higashi, A. Fujita, A. Inanobe et al., "An inwardly rectifying K+ channel, Kir4.1, expressed in astrocytes surrounds synapses and blood vessels in brain, " The American Journal of Physiology-Cell Physiology, vol. 281, no. 3, pp. C922-C931, 2001.
41. P. Kofuji, B. Biedermann, V. Siddharthan et al., "Kir potassium channel subunit expression in retinal glial cells: implications for spatial potassium buffering, " Glia, vol. 39, no. 3, pp. 292-303, 2002.
42. E. A. Newman, "Regional specialization of retinal glial cell membrane, " Nature, vol. 309, no. 5964, pp. 155-157, 1984.
43. E. A. Newman, "Distribution of potassium conductance in mammalian Müller (glial) cells: a comparative study, " The Journal of Neuroscience, vol. 7, no. 8, pp. 2423-2432, 1987.
44. C. G. Thomas, H. Tian, and J. S. Diamond, "The relative roles of diffusion and uptake in clearing synaptically released glutamate change during early postnatal development, " The Journal of Neuroscience, vol. 31, no. 12, pp. 4743-4754, 2011.
45. A. V. Tzingounis and J. I. Wadiche, "Glutamate transporters: confining runaway excitation by shaping synaptic transmission, " Nature Reviews Neuroscience, vol. 8, no. 12, pp. 935-947, 2007.
46. N. Zerangue andM. P. Kavanaugh, "Flux coupling in a neuronal glutamate transporter, " Nature, vol. 383, no. 6601, pp. 634-637, 1996.
47. C. Grewer, P. Balani, C. Weidenfeller, T. Bartusel, Z. Tao, and T. Rauen, "Individual subunits of the glutamate transporter EAAC1 homotrimer function independently of each other, " Biochemistry, vol. 44, no. 35, pp. 11913-11923, 2005.
48. H. P. Koch, R. L. Brown, and H. P. Larsson, "The glutamateactivated anion conductance in excitatory amino acid transporters is gated independently by the individual subunits, " The Journal of Neuroscience, vol. 27, no. 11, pp. 2943-2947, 2007.
49. L.M. Levy, K. P. Lehre, S. I. Walaas, N.C. Danbolt, and J. Storm-Mathisen, "Down-regulation of glial glutamate transporters after glutamatergic denervation in the rat brain, " European Journal of Neuroscience, vol. 7, no. 10, pp. 2036-2041, 1995.
50. K. Ullensvang, K. P. Lehre, J. Storm-Mathisen, and N. C. Danbolt, "Differential developmental expression of the two rat brain glutamate transporter proteins GLAST and GLT, " European Journal of Neuroscience, vol. 9, no. 8, pp. 1646-1655, 1997.
51. K. P. Lehre and N. C. Danbolt, "The number of glutamate transporter subtype molecules at glutamatergic synapses: chemical and stereological quantification in young adult rat brain, " The Journal of Neuroscience, vol. 18, no. 21, pp. 8751-8757, 1998.
52. F. A. Chaudhry, K. P. Lehre, M. Van Lookeren Campagne, O. P. Ottersen, N. C. Danbolt, and J. Storm-Mathisen, "Glutamate transporters in glial plasma membranes: highly differentiated localizations revealed by quantitative ultrastructural immunocytochemistry, " Neuron, vol. 15, no. 3, pp. 711-720, 1995.
53. D. E. Bergles and C. E. Jahr, "Synaptic activation of glutamate transporters in hippocampal astrocytes, " Neuron, vol. 19, no. 6, pp. 1297-1308, 1997.
54. D. E. Bergles and C. E. Jahr, "Glial contribution to glutamate uptake at Schaffer collateral-commissural synapses in the hippocampus, " Journal of Neuroscience, vol. 18, no. 19, pp. 7709-7716, 1998.
55. K. Tanaka, K. Watase, T. Manabe et al., "Epilepsy and exacerbation of brain injury in mice lacking the glutamate transporter GLT-1, " Science, vol. 276, no. 5319, pp. 1699-1702, 1997.
56. K. Watase, K. Hashimoto, M. Kano et al., "Motor discoordination and increased susceptibility to cerebellar injury in GLAST mutant mice, " European Journal of Neuroscience, vol. 10, no. 3, pp. 976-988, 1998.
57. C. Giaume, A. Koulakoff, L. Roux, D. Holcman, and N. Rouach, "Astroglial networks: a step further in neuroglial and gliovascular interactions, " Nature Reviews Neuroscience, vol. 11, no. 2, pp. 87-99, 2010.
58. J. C. Saez, V. M. Berthoud, M. C. Branes, A. D. Martinez, and E. C. Beyer, "Plasmamembrane channels formed by connexins: their regulation and functions, " Physiological Reviews, vol. 83, no. 4, pp. 1359-1400, 2003.
59. C. R. Rose and B. R. Ransom, "Gap junctions equalize intracellular Na+ concentration in astrocytes, " Glia, vol. 20, no. 4, pp. 299-307, 1997.
60. R. K. Orkand, J. G. Nicholls, and S. W. Kuffler, "Effect of nerve impulses on the membrane potential of glial cells in the central nervous system of amphibia, " Journal of Neurophysiology, vol. 29, no. 4, pp. 788-806, 1966.
61. A. Wallraff, R. Köhling, U. Heinemann, M. Theis, K. Willecke, and C. Steinhäuser, "The impact of astrocytic gap junctional coupling on potassium buffering in the hippocampus, " Journal of Neuroscience, vol. 26, no. 20, pp. 5438-5447, 2006.
62. E. Hansson, H. Muyderman, J. Leonova et al., "Astroglia and glutamate in physiology and pathology: aspects on glutamate transport, glutamate-induced cell swelling and gap-junction communication, " Neurochemistry International, vol. 37, no. 2-3, pp. 317-329, 2000.
63. M. A. Ozog, R. Siushansian, and C. C. G. Naus, "Blocked gap junctional coupling increases glutamate-induced neurotoxicity in neuron-astrocyte co-cultures, " Journal of Neuropathology and Experimental Neurology, vol. 61, no. 2, pp. 132-141, 2002.
64. E. A. Eugenin, D. Basilio, J. C. Sáez et al., "The role of gap junction channels during physiologic and pathologic conditions of the human central nervous system, " Journal of Neuroimmune Pharmacology, vol. 7, no. 3, pp. 499-518, 2012.
65. M. Figiel, C. Allritz, C. Lehmann, and J. Engele, "Gap junctional control of glial glutamate transporter expression, " Molecular and Cellular Neuroscience, vol. 35, no. 1, pp. 130-137, 2007.
66. C. Neusch, J. H. Weishaupt, and M. Bähr, "Kir channels in the CNS: emerging new roles and implications for neurological diseases, " Cell and Tissue Research, vol. 311, no. 2, pp. 131-138, 2003.
67. J. P. Ruppersberg, "Intracellular regulation of inward rectifierK+ channels, " Pflugers Archiv European Journal of Physiology, vol. 441, no. 1, pp. 1-11, 2000.
68. C. B. Ransom and H. Sontheimer, "Biophysical and pharmacological characterization of inwardly rectifying K+ currents in rat spinal cord astrocytes, " Journal of Neurophysiology, vol. 73, no. 1, pp. 333-346, 1995.
69. M. D. Mark and S. Herlitze, "G-protein mediated gating of inward-rectifier K+ channels, " European Journal of Biochemistry, vol. 267, no. 19, pp. 5830-5836, 2000.
70. L. Aguilar-Bryan and J. Bryan, "Molecular biology of adenosine triphosphate-sensitive potassiumchannels, " Endocrine Reviews, vol. 20, no. 2, pp. 101-135, 1999.
71. E. A. Nagelhus, Y. Horio, A. Inanobe et al., "Immunogold evidence suggests that coupling of K+ siphoning and water transport in rat retinal Muller cells is mediated by a coenrichment of Kir4.1 and AQP4 in specific membrane domains, " Glia, vol. 26, no. 1, pp. 47-54, 1999.
72. P. E. Fort, A. Sene, T. Pannicke et al., "Kir4.1 and AQP4 associate with Dp71-and utrophin-DAPs complexes in specific and defined microdomains of Müller retinal glial cell membrane, " Glia, vol. 56, no. 6, pp. 597-610, 2008.
73. B. Djukic, K. B. Casper, B. D. Philpot, L.-S. Chin, and K. D. McCarthy, "Conditional knock-out of Kir4.1 leads to glialmembrane depolarization, inhibition of potassium and glutamate uptake, and enhanced short-term synaptic potentiation, " The Journal of Neuroscience, vol. 27, no. 42, pp. 11354-11365, 2007.
74. H. Katagiri, K. Tanaka, and T. Manabe, "Requirement of appropriate glutamate concentrations in the synaptic cleft for hippocampal LTP induction, " European Journal ofNeuroscience, vol. 14, no. 3, pp. 547-553, 2001.
75. E. Tsvetkov, R.-M. Shin, andV. Y. Bolshakov, "Glutamate uptake determines pathway specificity of long-termpotentiation in the neural circuitry of fear conditioning, " Neuron, vol. 41, no. 1, pp. 139-151, 2004.
76. A. J. Bechtholt-Gompf, H. V. Walther, M. A. Adams, W. A. Carlezon, D. Ngür, and B. M. Cohen, "Blockade of astrocytic glutamate uptake in rats induces signs of anhedonia and impaired spatial memory, " Neuropsychopharmacology, vol. 35, no. 10, pp. 2049-2059, 2010.
77. T. Aida, J. Yoshida, M. Nomura et al., "Astroglial glutamate transporter deficiency increases synaptic excitability and leads to pathological repetitive behaviors in mice, " Neuropsychopharmacology, 2015.
78. G. Gegelashvili, N. C. Danbolt, and A. Schousboe, "Neuronal soluble factors differentially regulate the expression of the GLT1 and GLAST glutamate transporters in cultured astroglia, " Journal of Neurochemistry, vol. 69, no. 6, pp. 2612-2615, 1997.
79. R. A. Swanson, J. Liu, J.W. Miller et al., "Neuronal regulation of glutamate transporter subtype expression in astrocytes, " Journal of Neuroscience, vol. 17, no. 3, pp. 932-940, 1997.
80. M. Conradt andW. Stoffel, "Inhibition of the high-affinity brain glutamate transporter GLAST-1 via direct phosphorylation, " Journal of Neurochemistry, vol. 68, no. 3, pp. 1244-1251, 1997.
81. M. I. González, B. T. S. Susarla, andM. B. Robinson, "Evidence that protein kinase C+ interacts with and regulates the glial glutamate transporter GLT-1, " Journal of Neurochemistry, vol. 94, no. 5, pp. 1180-1188, 2005.
82. A. Kalandadze, Y. Wu, and M. B. Robinson, "Protein kinase C activation decreases cell surface expression of theGLT-1 subtype of glutamate transporter: requirement of a carboxyl-terminal domain and partial dependence on serine 486, " The Journal of Biological Chemistry, vol. 277, no. 48, pp. 45741-45750, 2002.
83. E. Foran, L. Rosenblum, A. Bogush, P. Pasinelli, and D. Trotti, "Sumoylation of the astroglial glutamate transporter EAAT2 governs its intracellular compartmentalization, " Glia, vol. 62, no. 8, pp. 1241-1253, 2014.
84. D. Trotti, B. L. Rizzini, D. Rossi et al., "Neuronal and glial glutamate transporters possess an SH-based redox regulatory mechanism, " European Journal of Neuroscience, vol. 9, no. 6, pp. 1236-1243, 1997.
85. C. Boehmer, M. Palmada, J. Rajamanickam, R. Schniepp, S. Amara, and F. Lang, "Post-translational regulation of EAAT2 function by co-expressed ubiquitin ligase Nedd4-2 is impacted by SGK kinases, " Journal of Neurochemistry, vol. 97, no. 4, pp. 911-921, 2006.
86. D. Trotti, A. Volterra, K. P. Lehre et al., "Arachidonic acid inhibits a purified and reconstituted glutamate transporter directly from the water phase and not via the phospholipid membrane, "The Journal of Biological Chemistry, vol. 270, no. 17, pp. 9890-9895, 1995.
87. S. Duan, C. M. Anderson, B. A. Stein, and R. A. Swanson, "Glutamate induces rapid upregulation of astrocyte glutamate transport and cell-surface expression of GLAST, " Journal of Neuroscience, vol. 19, no. 23, pp. 10193-10200, 1999.
88. A. M. Benediktsson, G. S. Marrs, J. C. Tu et al., "Neuronal activity regulates glutamate transporter dynamics in developing astrocytes, " Glia, vol. 60, no. 2, pp. 175-188, 2012.
89. I. M. González-González, N. García-Tardón, C. Giménez, and F. Zafra, "PKC-dependent endocytosis of the GLT1 glutamate transporter depends on ubiquitylation of lysines located in a Cterminal cluster, " Glia, vol. 56, no. 9, pp. 963-974, 2008.
90. J. Martinez-Villarreal, N. García Tardón, I. Ibáñez, C. Giménez, and F. Zafra, "Cell surface turnover of the glutamate transporter GLT-1 is mediated by ubiquitination/deubiquitination, " Glia, vol. 60, no. 9, pp. 1356-1365, 2012.
91. M. Stenovec, M. Kreft, S. Grilc, T. Pangršič, and R. Zorec, "EAAT2 density at the astrocyte plasma membrane and Ca2+-regulated exocytosis, " Molecular Membrane Biology, vol. 25, no. 3, pp. 203-215, 2008.
92. C. Murphy-Royal, J. P. Dupuis, J. A. Varela, and etal, "Surface diffusion of astrocytic glutamate transporters shapes synaptic transmission, " Nature Neuroscience, vol. 18, no. 2, pp. 219-226, 2015.
93. U. Pannasch, J. Sibille, and N. Rouach, "Dual electrophysiological recordings of synaptically-evoked astroglial and neuronal responses in acute hippocampal slices, " Journal of Visualized Experiments, no. 69, article e4418, 2012.
94. Y. Bernardinelli and J.-Y. Chatton, "Differential effects of glutamate transporter inhibitors on the global electrophysiological response of astrocytes to neuronal stimulation, " Brain Research, vol. 1240, pp. 47-53, 2008.
95. B. A. Clark and B. Barbour, "Currents evoked in Bergmann glial cells by parallel fibre stimulation in rat cerebellar slices, " The Journal of Physiology, vol. 502, no. 2, pp. 335-350, 1997.
96. C. Lüscher, R. C. Malenka, and R. A. Nicoll, "Monitoring glutamate release during LTP with glial transporter currents, " Neuron, vol. 21, no. 2, pp. 435-441, 1998.
97. U. Pannasch, M. Derangeon, O. Chever, and N. Rouach, "Astroglial gap junctions shape neuronal network activity, " Communicative & Integrative Biology, vol. 5, no. 3, pp. 248-254, 2012.
98. F. Amzica and M. Steriade, "Neuronal and glial membrane potentials during sleep and paroxysmal oscillations in the neocortex, " Journal of Neuroscience, vol. 20, no. 17, pp. 6648-6665, 2000.
99. F. Amzica, M. Massimini, and A. Manfridi, "Spatial buffering during slow and paroxysmal sleep oscillations in cortical networks of glial cells in vivo, " Journal of Neuroscience, vol. 22, no. 3, pp. 1042-1053, 2002.
100. O. Chever, B. Djukic, K. D. McCarthy, and F. Amzica, "Implication of Kir4.1 channel in excess potassium clearance: an in vivo study on anesthetized glial-conditional Kir4.1 knock-out mice, " Journal of Neuroscience, vol. 30, no. 47, pp. 15769-15777, 2010.
101. R. D'Ambrosio, D. S. Gordon, and H. Richard Winn, "Differential role of KIR channel and Na+/K+-pump in the regulation of extracellular K+ in rat hippocampus, " Journal of Neurophysiology, vol. 87, no. 1, pp. 87-102, 2002.
102. T. V. P. Bliss and G. L. Collingridge, "A synaptic model of memory: long-term potentiation in the hippocampus, " Nature, vol. 361, no. 6407, pp. 31-39, 1993.
103. C. G. Schipke, C. Ohlemeyer, M. Matyash, C. Nolte, H. Kettenmann, and F. Kirchhoff, "Astrocytes of the mouse neocortex express functional N-methyl-D-aspartate receptors, " The FASEB Journal, vol. 15, no. 7, pp. 1270-1272, 2001.
104. S. Manita, T. Suzuki, M. Inoue, Y. Kudo, and H. Miyakawa, "Paired-pulse ratio of synaptically induced transporter currents at hippocampal CA1 synapses is not related to release probability, " Brain Research, vol. 1154, no. 1, pp. 71-79, 2007.
105. T. Muller, T. Moller, T. Berger, J. Schnitzer, and H. Kettenmann, "Calcium entry through kainate receptors and resulting potassium-channel blockade in Bergmann glial cells, " Science, vol. 256, no. 5063, pp. 1563-16566, 1992.
106. 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.
107. J. S. Dittman, A. C. Kreitzer, and W. G. Regehr, "Interplay between facilitation, depression, and residual calcium at three presynaptic terminals, " Journal of Neuroscience, vol. 20, no. 4, pp. 1374-1385, 2000.
108. Y. Shen and D. J. Linden, "Long-term potentiation of neuronal glutamate transporters, " Neuron, vol. 46, no. 5, pp. 715-722, 2005.
109. J. Levenson, E. Weeber, J. C. Selcher, L. S. Kategayal, D. J. Sweatt, and A. Eskin, "Long-term potentiation and contextual fear conditioning increase neuronal glutamate uptake, " Nature Neuroscience, vol. 5, no. 2, pp. 155-161, 2002.
110. J.D. Rothstein, M. Dykes-Hoberg, C. A. Pardo et al., "Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate, " Neuron, vol. 16, no. 3, pp. 675-686, 1996.
111. E. A. Proper, G. Hoogland, S. M. Kappen et al., "Distribution of glutamate transporters in the hippocampus of patients with pharmaco-resistant temporal lobe epilepsy, " Brain, vol. 125, part 1, pp. 32-43, 2002.
112. H.-W. Shen, M. D. Scofield, H. Boger, M. Hensley, and P. W. Kalivas, "Synaptic glutamate spillover due to impaired glutamate uptake mediates heroin relapse, " Journal of Neuroscience, vol. 34, no. 16, pp. 5649-5657, 2014.
113. A. Massie, S. Goursaud, A. Schallier et al., "Time-dependent changes in GLT-1 functioning in striatum of hemi-Parkinson rats, " Neurochemistry International, vol. 57, no. 5, pp. 572-578, 2010.
114. A. Scimemi, J. S. Meabon, R. L. Woltjer, J. M. Sullivan, J. S. Diamond, and D. G. Cook, "Amyloid-1?42 slows clearance of synaptically released glutamate by mislocalizing astrocytic GLT-1, " The Journal of Neuroscience, vol. 33, no. 12, pp. 5312-5318, 2013.
115. R.D. Hawkins, T. E. Cohen, W. Greene, and E. R. Kandel, "Relationship between dishabituation, sensitization, and inhibition of the gill-and siphon-withdrawal reflex in Aplysia californica: effects of response measure, test time and training stimulus, " Behavioral Neuroscience, vol. 112, no. 1, pp. 24-38, 1998.
116. R.D. Hawkins, E. R. Kandel, and S. A. Siegelbaum, "Learning to modulate transmitter release: themes and variations in synaptic plasticity, " Annual Review of Neuroscience, vol. 16, pp. 625-665, 1993.
117. C. Boehmer, G. Henke, R. Schniepp et al., "Regulation of the glutamate transporter EAAT1 by the ubiquitin ligase Nedd4-2 and the serum and glucocorticoid-inducible kinase isoforms SGK1/3 and protein kinase B, " Journal of Neurochemistry, vol. 86, no. 5, pp. 1181-1188, 2003.
118. O. Khabour, J. Levenson, L. C. Lyons et al., "Coregulation of glutamate uptake and long-term sensitization in Aplysia, " Journal of Neuroscience, vol. 24, no. 40, pp. 8829-8837, 2004.
119. M. S. Collado, O. Khabour, D. Fioravante, J. H. Byrne, and A. Eskin, "Post-translational regulation of an Aplysia glutamate transporter during long-term facilitation, " Journal of Neurochemistry, vol. 108, no. 1, pp. 176-189, 2009.
120. M. S. Collado, L. C. Lyons, J. M. Levenson et al., "In vivo regulation of an Aplysia glutamate transporter, ApGT1, during long-term memory formation, " Journal of Neurochemistry, vol. 100, no. 5, pp. 1315-1328, 2007.
121. E. R. Kandel, "The molecular biology of memory storage: a dialogue between genes and synapses, " Science, vol. 294, no. 5544, pp. 1030-1038, 2001.
122. J. Zhou and M. L. Sutherland, "Glutamate transporter cluster formation in astrocytic processes regulates glutamate uptake activity, " Journal of Neuroscience, vol. 24, no. 28, pp. 6301-6306, 2004.
123. Y. Bernardinelli, J. Randall, E. Janett et al., "Activity-dependent structural plasticity of perisynaptic astrocytic domains promotes excitatory synapse stability, " Current Biology, vol. 24, no. 15, pp. 1679-1688, 2014.
124. A. Perez-Alvarez, M. Navarrete, A. Covelo, E. D. Martin, and A. Araque, "Structural and functional plasticity of astrocyte processes and dendritic spine interactions, " The Journal of Neuroscience, vol. 34, no. 38, pp. 12738-12744, 2014.