Selective depolarization of interneurons in the early posttraumatic dentate gyrus: Involvement of the Na+/K+-ATPase

Journal of Neurophysiology

Volumn 83, Issue 5, 2000, Pages 2916-2930

  Ross, Stephen T ^a   Soltesz, Ivan ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); POTASSIUM ION; SODIUM ION;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INJURY; CELL MEMBRANE DEPOLARIZATION; CONTROLLED STUDY; DENTATE GYRUS; ENTORHINAL CORTEX; ENZYME ACTIVITY; GRANULE CELL; HIPPOCAMPUS; INTERNEURON; ION EXCHANGE; NONHUMAN; PRIORITY JOURNAL; RAT;

EID: 0034117803     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.2000.83.5.2916     Document Type: Article

References (126)

1. ANDERSON, W. R., FRANCK, J. E., STAHL, W. L., AND MAKI, A. A. Na, K-ATPase is decreased in hippocampus of kainate-lesioned rats. Epilepsy Res. 17: 221-231, 1994.
2. ANKARCRONA, M., DYPBUKT, J. M., BONFOCO, E., ZHIVOTOVSKY, B., ORRENIUS, S., LIPTON, S. A., AND NICOTERA, P. Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function. Neuron 15: 961-973, 1995.
3. ANNEGERS, J. F., GRABOW, J. D., GROOVER, R. V., LAWS, E. R., JR., EIVEBACK, L. R., AND KURKLAND, L. T. Seizures after head trauma: a population study. Neurology 30: 683-689, 1980.
4. + channels. Trends Neurosci. 21: 288-294, 1998.
5. ASIKAINEN, I., KASTE, M., AND SARNA, S. Early and late posttraumatic seizures in traumatic brain injury rehabilitation patients: brain injury factors causing late seizures and influence of seizures on long-term outcome. Epilepsia 40: 584-589, 1999.
6. + transport in canine brain. Stroke 12: 726-730, 1981.
7. BEAL, M. F., HYMAN, B. T., AND KOROSHETZ, W. Do defects in mitochondrial energy metabolism underlie the pathology of neurodegenerative diseases? Trends Neurosci. 16: 125-131, 1993.
8. BINDER, L. M. Persisting symptoms after mild head injury: a review of the postconcussive syndrome. J. Clin. Exp. Neuropsychol. 8: 323-346, 1986.
9. f) in guinea-pig dissociated sinoatrial node cells. Br. J. Pharmacol. 110: 343-349, 1993.
10. +)-ATPase, cytochrome oxidase, and total protein in temporal lobe epilepsy. Epilepsia 36: 371-383, 1995.
11. BRONNER, C., MOUSLI, M., ELENO, N., AND LANDRY, Y. Resting plasma membrane potential of rat peritoneal mast cells is set predominantly by the sodium pump. Febs. Lett. 255: 401-404, 1989.
12. A receptor subunit expression and function in temporal lobe epilepsy. Nature Med. 4: 1166-1172, 1998.
13. BRUTON, C. The Neuropathology of Temporal Lobe Epilepsy. New York: Oxford, 1988.
14. BUCKMASTER, P. S. AND SCHWARTZKROIN, P. A. Interneurons and inhibition in the dentate gyrus of the rat in vivo. J. Neurosci. 15: 774-789, 1995.
15. BUHL, E. H., COBB, S. R., HALASY, K., AND SOMOGYI, P. Properties of unitary IPSPs evoked by anatomically identified basket cells in the rat hippocampus. Eur. J. Neurosci. 7: 1989-2004, 1995.
16. BUHL, E. H., HAN, Z. S., LORINCZI, Z., STEZHKA, V. V., KARNUP, S. V., AND SOMOGYI, P. Physiological properties of anatomically identified axo-axonic cells in the rat hippocampus. J. Neurophysiol. 71: 1289-1307, 1994.
17. BUHL, E. H., OTIS, T. S., AND MODY, I. Zinc-induced collapse of augmented inhibition by GABA in a temporal lobe epilepsy model. Science 271: 369-373, 1996.
18. BUZSÁKI, G. AND CHROBAK, J. J. Temporal structure in spatially organized neuronal ensembles: a role for interneuronal networks. Can. Opin. Neurobiol. 5: 504-510, 1995.
19. BUZSÁKI, G., LEUNG, L. W., AND VANRERWOLF, C. H. Cellular bases of hippocampal EEG in the behaving rat. Brain Res. 287: 139-171, 1983.
20. + ATPase. Eur. J. Neurosci. 7: 1674-1683, 1995.
21. CHAUHAN, N. B. AND SIEGEL, G. J. In situ analysis of Na, K-ATPase alpha1- and alpha3-isoform mRNAs in aging rat hippocampus. J. Neurochem. 66: 1742-1751, 1996.
22. CHEN, K., BARAM, T. Z., AND SOLTESZ, I. Febrile seizures in the developing brain result in persistent modification of neuronal excitability in limbic circuits. Nature Med. 5: 888-894, 1999.
23. CLAIBORNE, B. J., AMARAL, D. G., AND COWAN, W. M. A light and electron microscopic analysis of the mossy fibers of the rat dentate gyrus. J. Comp. Neurol. 246: 435-458, 1986.
24. COBB, S. R., BUHL, E. H., HALASY, K., PAULSEN, O., AND SOMOGYI, P. Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature 378: 75-78, 1995.
25. CORTEZ, S. C., MCINTOSH, T. K., AND NOBLE, L. J. Experimental fluid percussion brain injury: vascular disruption and neuronal and glial alterations. Brain Res. 482: 271-282, 1989.
26. COULTER, D. A., RAFIQ, A., SHUMATE, M., GONG, Q. Z., DELORENZO, R. J., AND LYETH, B. G. Brain injury-induced enhanced limbic epileptogenesis: anatomical and physiological parallels to an animal model of temporal lobe epilepsy. Epilepsy Res. 6: 81-91, 1996.
27. + gradients, and neurotransmitter amino acid levels in isolated rat brain synaptosomes. J. Neurochem. 49: 1229-1240, 1987.
28. +-homeostatis and altered electrophysiological properties of post-traumatic hippocampal glia. J. Neurosci. 19: 8152-8162, 1999.
29. D'AMBROSIO, R., WENZEL, J., SCHWARTZKROIN, P. A., MCKHANN, G. M., AND JANIGRO, D. Functional specialization and topographic segregation of hippocampal astrocytes. J. Neurosci. 18: 4425-4438, 1998.
30. + pump. In: Antiepileptic Drugs: Mechanisms of Action, edited by G. H. Glaser, J. K. Pentry, and D. M. Woodbury. New York: Raven, 1980, p. 85-126.
31. DIXON, C. E., LYETH, B. G., POVLISHOCK, J. T., FINDLING, R. L., HAMM, R. J., MARMAROU, A., YOUNG, H. F., AND HAYES, R. L. A fluid percussion model of experimental brain injury in the rat. J. Neurosurg. 67: 110-119, 1989.
32. ERECINSKA, M. AND SILVER, I. A. ATP and brain function. J. Cereb. Blood Flow Metab. 9: 2-19, 1989.
33. FADEN, A. I., DEMEDIUK, P., PANTER, S. S., AND VINK, R. The role of excitatory amino acids and NMDA receptors in traumatic brain injury. Science 244: 798-800, 1989.
34. FREUND, T. F. AND BUZSÁKI, G. Interneurons of the hippocampus. Hippocampus 6: 345-470, 1996.
35. + pump activation in rat hippocampal neurons. J. Neurophysiol. 68: 28-35, 1992a.
36. FUKUDA, A. AND PRINCE, D. A. Postnatal development of electrogenic sodium pump activity in rat hippocampal pyramidal neurons. Dev. Brain Res. 65: 101-114, 1992b.
37. GADSBY, D. C. AND NAKAO, M. Steady-state current-voltage relationship of the Na/K pump in guinea pig ventricular myocytes. J. Gen. Physiol. 94: 511-537, 1989.
38. GALLYAS, F., ZOLTAY, G., AND BALAS, I. An immediate light microscopic response of neuronal somata, dendrites and axons to contusing concussive head injury in the rat. Acta Neuropathol. 83: 394-401, 1992a.
39. GALLYAS, F., ZOLTAY, G., AND DAMES, W. Formation of "dark" (argyrophilic) neurons of various origin proceeds with a common mechanism of biophysical nature (a novel hypothesis). Acta Neuropathol. 83: 504-509, 1992b.
40. h) blocker ZD 7288 in hippocampal CA1 neurons. Pflügers Arch. 435: 99-106, 1997.
41. GLYNN, I. M. Annual review prize lecture. 'All hands to the sodium pump'. J. Physiol. (Lond.) 462: 1-30, 1993.
42. GOLDSTEIN, M. Traumatic brain injury: a silent epidemic. Ann. Neurol. 27: 327, 1990.
43. GRABER, K. D. AND PRINCE, D. A. Tetrodotoxin prevents post-traumatic epileptogenesis in rats. Ann. Neurol. 46: 234-242, 1999.
44. GRADY, M. S. AND LAM, A. M. Management of acute head injury. In: Anesthelic Management of Head Injury, edited by A. M. Lam. New York: McGraw-Hill, 1995, p. 87-100.
45. GRAHM, T. W., WILLIAMS, F. C., JR., HARRINGTON, T., AND SPETZLER, R. F. Civilian gunshot wounds to the head: a prospective study. Neurosurgery 27: 696-700, 1990.
46. + pump in epilepsy. Ann. Neurol. 16: S128-S134, 1984.
47. +-ATPaSe to focal epilepsy: a brief review. Epilepsy Res. 12: 141-149, 1992.
48. GUALTIERI, T. AND COX, D. R. The delayed neurobehavioural sequelae of traumatic brain injury. Brain Inj. 5: 219-232, 1991.
49. HAGLUND, M. M. AND SCHWARTZKROIN, P. A. Role of Na-K pump potassium regulation and IPSPs in seizures and spreading depression in immature rabbit hippocampal slices. J. Neurophysiol. 63: 225-239, 1990.
50. HAGLUND, M. M., STAHL, W. L., KUNKEL, D. D., AND SCHWARTZKROIN, P. A. Developmental and regional differences in the localization of Na, K-ATPase activity in the rabbit hippocampus. Brain Res. 343: 198-203, 1985.
51. HALASY, K. AND SOMOGYI, P. Subdivisions in the multiple GABAergic innervation of granule cells in the dentate gyrus of the rat hippocampus. Eur. J. Neurosci. 5: 411-429, 1993.
52. HAN, Z. S., BUHL, E. H., LORINCZI, Z., AND SOMOGYI, P. A high degree of spatial selectivity in the axonal and dendritic domains of physiologically identified local-circuit neurons in the dentate gyrus of the rat hippocampus. Eur. J. Neurosci. 5: 395-410, 1993.
53. HARRIS, N. C. AND CONSTANTI, A. Mechanism of block by ZD 7288 of the hyperpolarization-activated inward rectifying current in guinea pig substantia nigra neurons in vitro. J. Neurophysiol. 74: 2366-2378, 1995.
54. HARRISON, C. L. AND DIJKERS, M. Traumatic brain injury registries in the United States: an overview. Brain Inj. 6: 203-212, 1992.
55. HILLE, B. Ionic Channels of Excitable Membranes. Sunderland, MA: Sinauer, 1993.
56. A receptor activation in granule cells of the early postnatal dentate gyrus. J. Neurophysiol. 80: 2340-2351, 1998.
57. HOLLRIGEL, G. S. AND SOLTESZ, I. Slow kinetics of miniature IPSCs during early postnatal development in granule cells of the dentate gyrus. J. Neurosci. 17: 5119-5128, 1997.
58. HOLLRIGEL, G. S., TOTH, K., AND SOLTESZ, I. Neuroprotection by propofol in acute mechanical injury: role of GABAergic inhibition. J. Neurophysiol. 76: 2412-2422, 1996.
59. ISHIDA, Y. AND CHUSED, T. M. Lack of voltage sensitive potassium channels and generation of membrane potential by sodium potassium ATPase in murine T lymphocytes. J. Immunol. 151: 610-620, 1993.
60. + uptake in glia prevents long-term depression maintenance and causes epileptiform activity. J. Neurosci. 17: 2813-2824, 1997.
61. JENNETT, B. Epilepsy After Non-Missile Head Injuries. Oxford, UK: W. Heinemann Medical Books, 1975.
62. JENNETT, B. AND LEWIN, W. Traumatic epilepsy after closed head injuries. J. Neurol. Neurosurg. Psychiatry 23: 295-301, 1960.
63. JEWELL, E. A. AND LINGREL, J. B. Comparison of the substrate dependence properties of the rat Na, K-ATPase alpha 1, alpha 2, and alpha 3 isoforms expressed in HeLa cells. J. Biol. Chem. 266: 16925-16930, 1991.
64. JONES, S. W. On the resting potential of isolated frog sympathetic neurons. Neuron 3: 153-161, 1989.
65. KATAYAMA, Y., BECKER, D. P., TAMURA, T., AND HOVDA, D. A. Massive increases in extracellular potassium and the indiscriminate release of glutamate following concussive brain injury. J. Neurosurg. 73: 889-900, 1990.
66. KOH, D. S., GEIGER, J. R., JONAS, P., AND SAKMANN, B. Ca(2+)-permeable AMPA and NMDA receptor channels in basket cells of rat hippocampal dentate gyrus. J. Physiol. (Lond.) 485: 383-402, 1995.
67. KOH, D. S., JONAS, P., BRÄU, M. E., AND VOGEL, W. A TEA-insensitive flickering potassium channel active around the resting potential in myelinated nerve. J. Membr. Biol. 130: 149-162, 1992.
68. KYROZIS, A. AND REICHLING, D. B. Perforated-patch recording with gramicidin avoids artifactual changes in intracellular chloride concentration. J. Neurosci. Methods 57: 27-35, 1995.
69. LEES, G. J. Inhibition of sodium-potassium-ATPase: a potentially ubiquitous mechanism contributing to central nervous system neuropathology. Brain Res. Rev. 16: 283-300, 1991.
70. LEROUX, P. D. AND GRADY, M. S. Epidemology of head injury. In: Anesthetic Management of Head Injury, edited by A. M. Lam. New York: McGraw-Hill, 1995, p. 1-11.
71. LISMAN, J. E. AND IDIART, M. A. Storage of 7 ± 2 short-term memories in oscillatory subcycles. Science 267: 1512-1515, 1995.
72. LIU X. AND JONES, E. G. Alpha isoform of calcium-calmodulin dependent protein kinase II (CAM II kinase-alpha) restricted to excitatory synapses in the CA1 region of rat hippocampus. Neuroreport 8: 1475-1479, 1997.
73. LIU, X. B. AND JONES, E. G. Localization of alpha type II calcium calmodulin-dependent protein kinase at glutamatergic but not gamma-aminobutyric acid (GABAergic) synapses in thalamus and cerebral cortex. Proc. Natl. Acad. Sci. USA 93: 7332-7336, 1996.
74. LOWENSTEIN, D. H., THOMAS, M. J., SMITH, D. H., AND MCINTOSH, T. K. Selective vulnerability of dentate hilar neurons following traumatic brain injury: a potential mechanistic link between head trauma and disorders of the hippocampus. J. Neurosci. 12: 4846-4853, 1992.
75. LYETH, B. G., DIXON, C. E., JENKINS, L. W., HAMM, R. J., ALBERICO, A., YOUNG, H. F., STONNINGTON, H. H., AND HAYES, R. L. Effects of scopolamine treatment on long-term behavioral deficits following concussive brain injury to the rat. Brain Res. 452: 39-48, 1988.
76. MACCAFERRI, G. AND MCBAIN, C. J. Passive propagation of LTD to stratum oriens-alveus inhibitory neurons modulates the temporoammonic input to the hippocampal CA1 region. Neuron 15: 137-145, 1995.
77. h) and its contribution to pacemaker activity in rat CA1 hippocampal stratum oriens-alveus interneurones. J. Physiol. (Lond.) 497: 119-130, 1996.
78. MARGERISON, J. H. AND CORSELLIS, J. A. Epilepsy and the temporal lobes. A clinical, electroencephalographic and neuropathological study of the brain in epilepsy, with particular reference to the temporal lobes. Brain 89: 499-530, 1966.
79. MCBAIN, C. J. AND MACCAFERRI, G. Synaptic plasticity in hippocampal interneurons? A commentary. Can. J. Physiol. Pharmacol. 75: 488-494, 1997.
80. 2+-dependent conductance. J. Neurophysiol. 57: 496-509, 1987.
81. MCINTOSH, T. K., VINK, R., NOBLE, L., YAMAKAMI, I., FERNYAK, S., SOARES, H., AND FADEN, A. L. Traumatic brain injury in the rat: characterization of a lateral fluid-percussion model. Neuroscience 28: 233-244, 1989.
82. MCMAHON, L. L. AND KAUER, J. A. Hippocampal interneurons express a novel form of synaptic plasticity. Neuron 18: 295-305, 1997.
83. MILES, R., TÓTH, K., GULYÁS, A. I., HÁJOS, N., AND FREUND, T. F. Differences between somatic and dendritic inhibition in the hippocampus. Neuron 16: 815-823, 1996.
84. MOTT, D. D., TURNER, D. A., OKAZAKI, M. M., AND LEWIS, D. V. Interneurons of the dentate-hilus border of the rat dentate gyrus: morphological and electrophysiological heterogeneity. J. Neurosci. 17: 3990-4005, 1997.
85. NAGY, A. K., HOUSER, C. R., AND DELGADO-ESCUETA, A. V. Synaptosomal ATPase activities in temporal cortex and hippocampal formation of humans with focal epilepsy. Brain Res. 529: 192-201, 1990.
86. NAKAO, M. AND GADSBY, D. C. Voltage dependence of Na translocation by the Na/K pump. Nature 323: 628-630, 1986.
87. NEWMAN, E. A. Glial cell regulation of extracellular potassium. In: Neuroglia, edited by H. Kettenmann and B. R. Ransom. New York: Oxford Univ. Press, 1995, p. 717-731.
88. 2+ levels following cortical compression contusion trauma in rats. J. Cereb. Blood Flow Metab. 13: 183-192, 1993.
89. NUSSER, Z., HÁJOS, N., SOMOGYI, P., AND MODY, I. Increased number of synaptic GABA(A) receptors underlies potentiation at hippocampal inhibitory synapses. Nature 395: 172-177, 1998.
90. OBRENOVITCH, T. P. AND URENJAK, J. Is high extracellular glutamate the key to excitotoxicity in traumatic brain injury? J. Neurotrauma 14: 677-698, 1997.
91. OTIS, T. S., DE KONINCK, Y., AND MODY, I. Lasting potentiation of inhibition is associated with an increased number of gamma-aminobutyric acid type A receptors activated during miniature inhibitory postsynaptic currents. Proc. Natl. Acad. Sci USA 91: 7698-7702, 1994.
92. OTIS, T. S. AND MODY, I. Modulation of decay kinetics and frequency of GABAA receptor-mediated spontaneous inhibitory postsynaptic currents in hippocampal neurons. Neuroscience 49: 13-32, 1992.
93. PAPE, H. C. Queer current and pacemaker: the hyperpolarization-activated cation current in neurons. Annu. Rev. Physiol. 58: 299-327, 1996.
94. PENG, L., MARTIN-VASALLO, P., AND SWEADNER. K. J. Isoforms of Na, K-ATPase alpha and beta subunits in the rat cerebellum and in granule cell cultures. J. Neurosci. 17: 3488-3502, 1997.
95. POVLISHOCK, J. T., HAYES, R. L., MICHEL, M. E., AND MCINTOSH, T. K. Workshop on animal models of traumatic brain injury. J. Neurotrauma 11: 723-732, 1994.
96. PRASAD, M. R., DHILLON, H. S., CARBARY, T., DEMPSEY, R. J., AND SCHEFF, S. W. Enhanced phosphodiestric breakdown of phosphatidylinositol bisphosphate after experimental brain injury. J. Neurochem. 63: 773-776, 1994.
97. PRIEBE, L., FRIEDRICH, M., AND BENNDORF, K. Functional interaction between K(ATP) channels and the Na(+)-K(+) pump in metabolically inhibited heart cells of the guinea-pig. J. Physiol. (Lond.) 492: 405-417, 1996.
98. REMPEL-CLOWER, N. L., ZOLA, S. M., SQUIRE, L. R., AND AMARAL, D. G. Three cases of enduring memory impairment after bilateral damage limited to the hippocampal formation. J. Neurosci. 16: 5233-5255, 1996.
99. RETZ, K. C. AND COYLE, J. T. Effects of kainic acid on high-energy metabolites in the mouse striatum. J. Neurochem. 38: 196-203, 1982.
100. ROTHMAN, S. M. AND OLNEY, J. W. Glutamate and the pathophysiology of hypoxic-ischemic brain damage. Ann. Neurol. 19: 105-111, 1986.
101. SALAZAR, A. Traumatic brain injury: the continuing epidemic. In: Challenges in Neurology, edited by V. C. Hachinski. Philadelphia, PA: Davis, 1992, p. 55-67.
102. SALAZAR, A., JABBARI, B., VANCE, S., GRAFMAN, J., AND AMIN, D. Epilepsy after penetrating head injury. I. Clinical correlates. Neurology 35: 1406-1414, 1985.
103. SENATOROV, V. V. AND HU, B. Differential Na(+)-K(+)-ATPase activity in rat lemniscal and non-lemniscal auditory thalami. J. Physiol. (Lond.) 502: 387-395, 1997.
104. SENATOROV, V. V., MOONEY, D., AND HU, B. The electrogenic effects of Na(+)-K(+)-ATPase in rat auditory thalamus. J. Physiol. (Lond.) 502: 375-385, 1997.
105. 2+ signaling pathway in GABAergic neurons of the hippocampus. Proc. Natl. Acad. Sci. USA 95: 3245-3250, 1998.
106. SOLTESZ, I. AND DESCHÊNES. M. Low- and high-frequency membrane-potential oscillations during theta activity in morphologically identified neurons of the rat hippocampus during ketamine-xylazine anesthesia. J. Neurophysiol. 70: 97-116, 1993.
107. SOLTESZ, I., LICHTOWLER, S., LERESCHE, N., JASSIK-GERSCHENFELD, D., POLLARD, C. E., AND CRUNELLI, V. Two inward currents and the transformation of low-frequency oscillations of rat and cat thalamocortical cells. J. Physiol. (Lond.) 441: 175-197, 1991.
108. SOLTESZ, I. AND MODY, I. Patch-clamp recordings reveal powerful GABAergic inhibition in dentate hilar neurons. J. Neurosci. 14: 2365-2376, 1994.
109. 2+-dependent plasticity of miniature inhibitory postsynaptic currents after amputation of dendrites in central neurons. J. Neurophysiol. 73: 1763-1773, 1995.
110. SOLTESZ, I., SMETTERS, D. K., AND MODY, I. Tonic inhibition originates from synapses close to the soma. Neuron 14: 1273-1283, 1995.
111. STALEY, K. J., OTIS, T. S., AND MODY, I. Membrane properties of dentate gyms granule cells: comparison of sharp microelectrode and whole-cell recordings. J. Neurophysiol. 67: 1346-1358, 1992.
112. STORM, J. F. Potassium currents in hippocampal pyramidal cells. Prog. Brain Res. 83: 161-187, 1990.
113. STUART, G. J., DODT, H. U., AND SAKMANN, B. Patch-clamp recordings from the soma and dendrites of neurons in brain slices using infrared video microscopy. Pflügers Arch. 423: 511-518, 1993.
114. SULLIVAN, P. G., KELLER, J. N., MATTSON, M. P., AND SCHEFF, S. W. Traumatic brain injury alters synaptic homeostasis: Implications for impaired mitochondrial and transport function. J. Neurotrauma 15: 789-798, 1998.
115. TAVALIN, S. J., ELLIS, E. F., AND SATIN, L. S. Mechanical perturbation of cultured cortical neurons reveals a stretch-induced delayed depolarization. J. Neurophysiol. 74: 2767-2773, 1995.
116. TAVALIN, S. J., ELLIS, E. F., AND SATIN, L. S. Inhibition of the electrogenic Na pump underlies delayed depolarization of cortical neurons after mechanical injury or glutamate. J. Neurophysiol. 77: 632-638, 1997.
117. THOMAS, R. Electrogenic sodium pump in nerve and muscle cells. Physiol. Rev. 52: 563-594, 1972.
118. THOMPSON, S. M. AND PRINCE, D. A. Activation of electrogenic sodium pump in hippocampal CA1 neurons following glutamate-induced depolarization. J. Neurophysiol. 56: 507-522, 1986.
119. TOTH, Z., HOLLRIGEL, G. S., GORCS, T., AND SOLTESZ, I. Instantaneous perturbation of interneuronal networks by a pressure wave-transient delivered to the neocortex. J. Neurosci. 17: 8106-8117, 1997.
120. TRAUB, R. D., SPRUSTON, N., SOLTESZ, I., KONNERTH, A., WHITTINGTON, M. A., AND JEFFEREYS, J.G.R. Gamma-frequency oscillations: a neuronal population phenomenon regulated by synaptic and intrinsic cellular processes. Prog. Neurobiol. 55: 563-575, 1998.
121. TROTIER, D. AND DØVING, K. B. Direct influence of the sodium pump on the membrane potential of vomeronasal chemoreceptor neurones in frog. J. Physiol. (Lond.) 490: 611-621, 1996.
122. WALKER, M. C. AND KULLMANN, D. M. Febrile convulsions: a 'benign' condition? Nature Med. 5: 871-872, 1999.
123. WHITTAM, R. The dependence of the respiration of brain cortex on active cation transport. Biochem. J. 82: 205-212, 1962.
124. WILLMORE, L. J. Prophylactic treatment. In: Epilepsy: A Comprehensive Textbook, edited by J. Engel and T. A. Pedley. Philadelphia, PA: Lippincott-Raven Publishers, 1997, p. 1333-1337.
125. YLINEN, A., SOLTESZ, I., BRAGIN, A., PENTONNEN, M., SIK, A., AND BUZSÁKI, G. Intracellular correlates of hippocampal theta rhythm in identified pyramidal cells, granule cells and basket cells. Hippocampus 5: 78-91, 1995.
126. ZAWAR, C., PLANT, T. D., SCHIRRA, C., KONNERTH, A., AND NEUMCKE, B. Cell-type specific expression of ATP-sensitive potassium channels in the rat hippocampus. J. Physiol. (Lond.) 514: 327-341, 1999.