Functional, metabolic, and synaptic changes after seizures as potential targets for antiepileptic therapy

Epilepsy and Behavior

Volumn 19, Issue 2, 2010, Pages 105-113

  Löscher, Wolfgang ^a,b   Köhling, Rüdiger ^c  

^a UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

^b CENTER FOR SYSTEMS NEUROSCIENCE   (Germany)

^c UNIVERSITY OF ROSTOCK   (Germany)

Author keywords

Adenosine; Endocannabinoids; Endogenous anticonvulsants; Epilepsy; GABA; Kindling; NPY; PH; Seizure arrest; Seizure termination

Indexed keywords

4 AMINOBUTYRIC ACID; ADENOSINE; ANTICONVULSIVE AGENT; CARBAMAZEPINE; DOPAMINE; GLUTAMIC ACID; MONOAMINE; NEUROPEPTIDE Y; NORADRENALIN; PHENOBARBITAL; SEROTONIN; VALPROIC ACID;

DISEASE DURATION; DISEASE SEVERITY; DRUG MECHANISM; DRUG TARGETING; EPILEPSY; HUMAN; KINDLING; NERVE CELL EXCITABILITY; NEUROMODULATION; NONHUMAN; PH; REVIEW; SEIZURE; SYNAPSE;

ANIMALS; ANTICONVULSANTS; BRAIN; HUMANS; KINDLING, NEUROLOGIC; NEURONS; SEIZURES; SYNAPSES;

EID: 77957337142     PISSN: 15255050     EISSN: 15255069     Source Type: Journal    
DOI: 10.1016/j.yebeh.2010.06.035     Document Type: Review

References (131)

1. Dragunow M. Endogenous anticonvulsant substances. Neurosci Biobehav Rev 1986, 10:229-244.
2. Lado F.A., Moshe S.L. How do seizures stop?. Epilepsia 2008, 49:1651-1664.
3. Engel J.J., Dichter M.A., Schwartzkroin P.A. Basic mechanisms of human epilepsy. Epilepsy: a comprehensive textbook 2008, 495-507. Lippincott Williams & Wilkins, Philadelphia. J.J. Engel, T.A. Pedley (Eds.).
4. Toman J.E.P., Swinyard E.A., Goodman L.S. Properties of maximal seizures and their alteration by anticonvulsant drugs and other agents. J Neurophysiol 1946, 9:231-239.
5. Herberg L.J., Tress K.H., Blundell J.E. Raising the threshold in experimental epilepsy by hypothalamic and septal stimulation and by audiogenic seizures. Brain 1969, 92:313-328.
6. Essig C.F., Flanary H.G. The importance of the convulsion in occurrence and rate of development of electroconvulsive threshold elevation. Exp Neurol 1966, 14:448-452.
7. Nutt D.J., Cowen P.J., Green A.R. Studies on the post-ictal rise in seizure threshold. Eur J Pharmacol 1981, 71:287-295.
8. Nutt D.J., Cowen P.J., Green A.R. On the measurement in rats of the convulsant effect of drugs and the changes which follow electroconvulsive shock. Neuropharmacology 1980, 19:1017-1023.
9. 3H]diazepam binding in rat brain following repeated electroconvulsive shock. J Neural Transm 1983, 56:3-12.
10. Bowdler J.M., Green A.R. Regional rat brain benzodiazepine receptor number and gamma-aminobutyric acid concentration following a convulsion. Br J Pharmacol 1982, 76:291-298.
11. Green A.R. Changes in gamma-aminobutyric acid biochemistry and seizure threshold. Ann NY Acad Sci 1986, 462:105-119.
12. Green A.R., Vincent N.D. The effect of repeated electroconvulsive shock on GABA synthesis and release in regions of rat brain. Br J Pharmacol 1987, 92:19-24.
13. Green A.R., Metz A., Minchin M.C.W., Vincent N.D. Inhibition of the rate of GABA synthesis in regions of rat brain following a convulsion. Br J Pharmacol 1987, 92:5-11.
14. Green A.R., Minchin M.C., Vincent N.D. Inhibition of GABA release from slices prepared from several brain regions of rats at various times following a convulsion. Br J Pharmacol 1987, 92:13-18.
15. Sackeim H.A., Devanand D.P., Prudic J. Stimulus intensity, seizure threshold, and seizure duration: impact on the efficacy and safety of electroconvulsive therapy. Psychiatr Clin North Am 1991, 14:803-843.
16. Reisner A.D. The electroconvulsive therapy controversy: evidence and ethics. Neuropsychol Rev 2003, 13:199-219.
17. Paul S.M., Skolnick P. Rapid changes in brain benzodiazepine receptors after experimental seizures. Science 1978, 202:892-894.
18. Tuff L.P., Racine R.J., Adamec R. The effects of kindling on GABA-mediated inhibition in the dentate gyrus of the rat: I. Paired-pulse depression. Brain Res 1983, 277:79-90.
19. Löscher W., Frey H.-H. Postictal refractoriness associated with reduction of glutamic acid decarboxylase in discrete brain regions in epilepsy-prone gerbils. Biochem Pharmacol 1987, 36:2695-2699.
20. Sasahira M., Lowry T., Simon R.P., Greenberg D.A. Epileptic tolerance: prior seizures protect against seizure-induced neuronal injury. Neurosci Lett 1995, 185:95-98.
21. Kelly M.E., McIntyre D.C. Hippocampal kindling protects several structures from the neuronal damage resulting from kainic acid-induced status epilepticus. Brain Res 1994, 634:245-256.
22. Kondratyev A., Sahibzada N., Gale K. Electroconvulsive shock exposure prevents neuronal apoptosis after kainic acid-evoked status epilepticus. Brain Res Mol Brain Res 2001, 91:1-13.
23. Najm I.M., Hadam J., Ckakraverty D., et al. A short episode of seizure activity protects from status epilepticus-induced neuronal damage in rat brain. Brain Res 1998, 810:72-75.
24. Borges K., Shaw R., Dingledine R. Gene expression changes after seizure preconditioning in the three major hippocampal cell layers. Neurobiol Dis 2007, 26:66-77.
25. Hatazaki S., Bellver-Estelles C., Jimenez-Mateos E.M., et al. Microarray profile of seizure damage-refractory hippocampal CA3 in a mouse model of epileptic preconditioning. Neuroscience 2007, 150:467-477.
26. Andre V., Ferrandon A., Marescaux C., Nehlig A. The lesional and epileptogenic consequences of lithium-pilocarpine-induced status epilepticus are affected by previous exposure to isolated seizures: effects of amygdala kindling and maximal electroshocks. Neuroscience 2000, 99:469-481.
27. Jimenez-Mateos E.M., Hatazaki S., Johnson M.B., et al. Hippocampal transcriptome after status epilepticus in mice rendered seizure damage-tolerant by epileptic preconditioning features suppressed calcium and neuronal excitability pathways. Neurobiol Dis 2008, 32:442-453.
28. Bengzon J., Kokaia Z., Elmer E., Nanobashvili A., Kokaia M., Lindvall O. Apoptosis and proliferation of dentate gyrus neurons after single and intermittent limbic seizures. Proc Natl Acad Sci USA 1997, 94:10432-10437.
29. Pinel J.P., Van Oot P.H. Generality of the kindling phenomenon: some clinical implications. Can J Neurol Sci 1975, 2:467-475.
30. Nutt D.J., Cowen P.J., Batts C.C., Grahame-Smith D.G., Green A.R. Repeated administration of subconvulsant doses of GABA antagonist drugs: I. Effect on seizure threshold (kindling). Psychopharmacology (Berl) 1982, 76:84-87.
31. Kurinji S., Andrade C. ECS seizure threshold: normal variations, and kindling effects of subconvulsive stimuli. J ECT 2003, 19:31-37.
32. Gowers W.R. Epilepsy and other chronic convulsive diseases 1881, Wood, London.
33. Goddard G.V., McIntyre D.C., Leech C.K. A permanent change in brain function resulting from daily electrical stimulation. Exp Neurol 1969, 25:295-330.
34. McIntyre D.C., Poulter M.O., Gilby K. Kindling: some old and some new. Epilepsy Res 2002, 50:79-92.
35. Racine R.J. Modification of seizure activity by electrical stimulation: I. After-discharge threshold. Electroencephalogr Clin Neurophysiol 1972, 32:269-279.
36. Stripling J.S., Russell R.D. Twenty-four-hour post-seizure inhibition during limbic kindling requires seizure generalization. Neurosci Lett 1989, 99:208-213.
37. Freeman F.G., Jarvis M.F. The effect of interstimulation interval on the assessment and stability of kindled seizure threshold. Brain Res Bull 1981, 7:629-633.
38. Löscher W., Jäckel R., Müller F. Anticonvulsant and proconvulsant effects of inhibitors of GABA degradation in the amygdala-kindling model. Eur J Pharmacol 1989, 163:1-14.
39. Racine R.J. Modification of seizure activity by electrical stimulation: II. Motor seizure. Electroencephalogr Clin Neurophysiol 1972, 32:281-294.
40. Löscher W., Hönack D., Hashem A. Anticonvulsant efficacy of clonazepam and the beta-carboline ZK 93423 during chronic treatment in amygdala-kindled rats. Eur J Pharmacol 1987, 143:403-414.
41. Handforth A. Postseizure inhibition of kindled seizures by electroconvulsive shock. Exp Neurol 1982, 78:483-491.
42. Mucha R.F., Pinel J.P.J. Postseizure inhibition of kindled seizures. Exp Neurol 1977, 54:266-282.
43. Francis A., Fochtmann L. Genetic variation in immediate and delayed postictal refractory period in rats. Brain Res 1996, 721:150-154.
44. Mace J.A., Burnham W.M. The effect of repeated seizures on anticonvulsant drug response in the kindling model. Electroencephalogr Clin Neurophysiol 1987, 67:171-175.
45. Löscher W., Hönack D. The effect of interstimulation interval on the assessment of anticonvulsant drug potency in fully kindled rats. Epilepsy Res 1990, 7:182-196.
46. Löscher W., Fiedler M. Repeated acute testing of anticonvulsant drugs in amygdala kindled rats: increase in anticonvulsant but decrease in adverse effect potential. Epilepsia 2000, 41:516-528.
47. Engel J., Ackermann R.F., Caldecott-Hazard S., Kuhl D.E. Epileptic activation of antagonistic systems may explain paradoxical features of experimental and human epilepsy: a review and hypothesis. Kindling 2 1981, 193-217. Raven Press, New York. J.A. Wada (Ed.).
48. Schmidt D., Löscher W. Drug resistance in epilepsy: putative neurobiologic and clinical mechanisms. Epilepsia 2005, 46:858-877.
49. Sutula T.P., Hagen J., Pitkänen A. Do epileptic seizures damage the brain?. Curr Opin Neurol 2003, 16:189-195.
50. Löscher W, Brandt C. Prevention or modification of epileptogenesis after brain insults: experimental approaches and translational research. in press.
51. Spencer S.S., Spencer D.D. Implications of seizure termination location in temporal lobe epilepsy. Epilepsia 1996, 37:455-458.
52. Suffczynski P., Lopes da Silva F.H., Parra J., et al. Dynamics of epileptic phenomena determined from statistics of ictal transitions. IEEE Trans Biomed Eng 2006, 53:524-532.
53. Kudela P., Franaszczuk P.J., Bergey G.K. Reduction of intracellular calcium removal rate can explain changes in seizure dynamics: studies in neuronal network models. Epilepsy Res 2003, 57:95-109.
54. Doman G., Pelligra R. A unifying concept of seizure onset and termination. Med Hypoth 2004, 62:740-745.
55. Yamada K., Ji J.J., Yuan H., et al. Protective role of ATP-sensitive potassium channels in hypoxia-induced generalized seizure. Science 2001, 292:1543-1546.
56. Kirchner A., Velísková J., Velísek L. Differential effects of low glucose concentrations on seizures and epileptiform activity in vivo and in vitro. Eur J Neurosci 2006, 23:1512-1522.
57. 2 and pH: changes during convulsive activity and their significance for spontaneous arrest of seizures. Epilepsia 1972, 13:699-725.
58. Namba H., Iwasa H., Kubota M., et al. Local cerebral glucose utilization in the postictal phase of amygdaloid kindled rats. Brain Res 1989, 486:221-227.
59. Staley K.J., Longacher M., Bains J.S., Yee A. Presynaptic modulation of CA3 network activity. Nat Neurosci 1998, 1:201-209.
60. Jones J., Stubblefield E.A., Benke T.A., Staley K.J. Desynchronization of glutamate release prolongs synchronous CA3 network activity. J Neurophysiol 2007, 97:3812-3818.
61. Lopantsev V., Both M., Draguhn A. Rapid plasticity at inhibitory and excitatory synapses in the hippocampus induced by ictal epileptiform discharges. Eur J Neurosci 2009, 29:1153-1164.
62. Domann R., Uhlig S., Dorn T., Witte O.W. Participation of interneurons in penicillin-induced epileptic discharges. Exp Brain Res 1991, 83:683-686.
63. Prince D.A., Wilder B.J. Control mechanisms in cortical epileptogenic foci: "surround" inhibition. Arch Neurol 1967, 16:194-202.
64. 2+-free medium: the role of GABAa inhibition. Epilepsy Res 1988, 2:239-245.
65. Khazipov R., Holmes G.L. Synchronization of kainate-induced epileptic activity via GABAergic inhibition in the superfused rat hippocampus in vivo. J Neurosci 2003, 23:5337-5341.
66. Köhling R., Lücke A., Straub H., et al. Spontaneous sharp waves in human neocortical slices excised from epileptic patients. Brain 1998, 121:1073-1087.
67. Köhling R., Vreugdenhil M., Bracci E., Jefferys J.G. Ictal epileptiform activity is facilitated by hippocampal GABAA receptor-mediated oscillations. J Neurosci 2000, 20:6820-6829.
68. Cohen I., Navarro V., Clemenceau S., Baulac M., Miles R. On the origin of interictal activity in human temporal lobe epilepsy in vitro. Science 2002, 298:1418-1421.
69. Bragin D.E., Sanderson J.L., Peterson S., Connor J.A., Müller W.S. Development of epileptiform excitability in the deep entorhinal cortex after status epilepticus. Eur J Neurosci 2009, 30:611-624.
70. Pathak H.R., Weissinger F., Terunuma M., et al. Disrupted dentate granule cell chloride regulation enhances synaptic excitability during development of temporal lobe epilepsy. J Neurosci 2007, 27:14012-14022.
71. Khalilov I., Holmes G.L., Ben-Ari Y. In vitro formation of a secondary epileptogenic mirror focus by interhippocampal propagation of seizures. Nat Neurosci 2003, 6:1079-1085.
72. Le Van Quyen M., Khalilov I., Ben-Ari Y. The dark side of high-frequency oscillations in the developing brain. Trends Neurosci 2006, 29:419-427.
73. Stell B.M., Brickley S.G., Tang C.Y., Farrant M., Mody I. Neuroactive steroids reduce neuronal excitability by selectively enhancing tonic inhibition mediated by delta subunit-containing GABAA receptors. Proc Natl Acad Sci USA 2003, 100:14439-14444.
74. Lawrence C., Martin B.S., Sun C., Williamson J., Kapur J. Endogenous neurosteroid synthesis modulates seizure frequency. Ann Neurol 2010, 67:689-693.
75. Gorter J.A., van Vliet E.A., Aronica E., et al. Potential new antiepileptogenic targets indicated by microarray analysis in a rat model for temporal lobe epilepsy. J Neurosci 2006, 26:11083-11110.
76. 2+ in rat hippocampal slices depends on gap junctional coupling. Neuroscience 2001, 105:579-587.
77. Gigout S., Louvel J., Kawasaki H., et al. Effects of gap junction blockers on human neocortical synchronization. Neurobiol Dis 2006, 22:496-508.
78. + buffering in the hippocampus. J Neurosci 2006, 26:5438-5447.
79. Roopun A.K., Simonotto J.D., Pierce M.L., et al. A nonsynaptic mechanism underlying interictal discharges in human epileptic neocortex. Proc Natl Acad Sci USA 2010, 107:338-343.
80. De Curtis M., Manfridi A., Biella G. Activity-dependent pH shifts and periodic recurrence of spontaneous interictal spikes in a model of focal epileptogenesis. J Neurosci 1998, 18:7543-7551.
81. Timofeev I., Grenier F., Steriade M. Contribution of intrinsic neuronal factors in the generation of cortically driven electrographic seizures. J Neurophysiol 2004, 92:1133-1143.
82. Kirschstein T., Schulz R., Köhling R. Network excitability critically depends on Sk-dependent AHP-currents in a model of chronic TLE. Epilepsia 2009, 50(Suppl. 4):96.
83. Isokawa M. Decrement of GABAA receptor-mediated inhibitory postsynaptic currents in dentate granule cells in epileptic hippocampus. J Neurophysiol 1996, 75:1901-1908.
84. Stegen M., Young C.C., Haas C.A., Zentner J., Wolfart J. Increased leak conductance in dentate gyrus granule cells of temporal lobe epilepsy patients with Ammon's horn sclerosis. Epilepsia 2009, 50:646-653.
85. Isokawa M. Decreased time constant in hippocampal dentate granulelike cells in pilocarpine treated rats with progressive seizure frequencies. Brain Res 1996, 718:169-175.
86. Bikson M., Hahn P.J., Fox J.E., Jefferys J.G. Depolarization block of neurons during maintenance of electrographic seizures. J Neurophysiol 2003, 90:2402-2408.
87. Lux H.D., Heinemann U., Dietzel I. Ionic changes and alterations in the size of the extracellular space during epileptic activity. Adv Neurol 1986, 44:619-639.
88. Pinto D.J., Patrick S.L., Huang W.C., Connors B.W. Initiation, propagation, and termination of epileptiform activity in rodent neocortex in vitro involve distinct mechanisms. J Neurosci 2005, 25:8131-8140.
89. Avoli M., Barbarosie M., Lücke A., Nagao T., Lopantsev V., Köhling R. Synchronous GABA-mediated potentials and epileptiform discharges in the rat limbic system in vitro. J Neurosci 1996, 16:3912-3924.
90. Köhling R., Lücke A., Nagao T., Speckmann E.J., Avoli M. Extracellular potassium elevations in the hippocampus of rats with long-term pilocarpine seizures. Neurosci Lett 1995, 201:87-91.
91. Cohen J.E., Fields R.D. Extracellular calcium depletion in synaptic transmission. Neuroscientist 2004, 10:12-17.
92. 2+-induces seizures in combined entorhinal cortex-hippocampal slices. Exp Brain Res 1994, 101:44-52.
93. Velísek L. Extracellular acidosis and high levels of carbon dioxide suppress synaptic transmission and prevent the induction of long-term potentiation in the CA1 region of rat hippocampal slices. Hippocampus 1998, 8:24-32.
94. Ziemann A.E., Schnizler M.K., Albert G.W., et al. Seizure termination by acidosis depends on ASIC1a. Nat Neurosci 2008, 11:816-822.
95. Xiong Z.Q., Saggau P., Stringer J.L. Activity-dependent intracellular acidification correlates with the duration of seizure activity. J Neurosci 2000, 20:1290-1296.
96. Schuchmann S., Schmitz D., Rivera C., et al. Experimental febrile seizures are precipitated by a hyperthermia-induced respiratory alkalosis. Nat Med 2006, 12:817-823.
97. Lewin E, Bleck V. Electroshock seizures in mice: effect on brain adenosine and its metabolites. Epilepsia 1981;22:577-81.
98. Young D., Dragunow M. Status epilepticus may be caused by loss of adenosine anticonvulsant mechanisms. Neuroscience 1994, 58:245-261.
99. Marksteiner J., Sperk G., Maas D. Differential increases in brain levels of neuropeptide Y and vasoactive intestinal polypeptide after kainic acid-induced seizures in the rat. Naunyn Schmiedebergs Arch Pharmacol 1989, 339:173-177.
100. Tu B., Timofeeva O., Jiao Y., Nadler J.V. Spontaneous release of neuropeptide Y tonically inhibits recurrent mossy fiber synaptic transmission in epileptic brain. J Neurosci 2005, 25:1718-1729.
101. Jankowsky J.L., Patterson P.H. Differential regulation of cytokine expression following pilocarpine-induced seizure. Exp Neurol 1999, 159:333-346.
102. De Simoni M.G., Perego C., Ravizza T., et al. Inflammatory cytokines and related genes are induced in the rat hippocampus by limbic status epilepticus. Eur J Neurosci 2000, 12:2623-2633.
103. Vezzani A., Moneta D., Richichi C., et al. Functional role of inflammatory cytokines and antiinflammatory molecules in seizures and epileptogenesis. Epilepsia 2002, 43:30-35.
104. Jakubs K., Bonde S., Iosif R.E., et al. Inflammation regulates functional integration of neurons born in adult brain. J Neurosci 2008, 28:12477-12488.
105. Wasterlain C.G., Mazarati A.M., Naylor D., et al. Short-term plasticity of hippocampal neuropeptides and neuronal circuitry in experimental status epilepticus. Epilepsia 2002, 43:20-29.
106. Koepp M.J., Richardson M.P., Brooks D.J., Duncan J.S. Focal cortical release of endogenous opioids during reading-induced seizures. Lancet 1998, 352:952-955.
107. Hammers A., Asselin M.C., Hinz R., et al. Upregulation of opioid receptor binding following spontaneous epileptic seizures. Brain 2007, 130:1009-1016.
108. Loacker S., Sayyah M., Wittmann W., Herzog H., Schwarzer C. Endogenous dynorphin in epileptogenesis and epilepsy: anticonvulsant net effect via kappa opioid receptors. Brain 2007, 130:1017-1028.
109. Avoli M., Köhling R., Barbarosie M. Anoxia blocks the presynaptic control of GABA release at inhibitory terminals in the rat hippocampus. Neuroscience 1996, 75:999-1002.
110. Zhang H.N., Ko M.C. Seizure activity involved in the up-regulation of BDNF mRNA expression by activation of central mu opioid receptors. Neuroscience 2009, 161:301-310.
111. Wada J.A., Sato M., Corcoran M.E. Antiepileptic properties of 9-tetrahydrocannabinol. Exp Neurol 1973, 39:157-165.
112. Wada J.A., Wake A., Sato M., Corcoran M.E. Antiepileptic and prophylactic effects of tetrahydrocannabinols in amygdaloid kindled cats. Epilepsia 1975, 16:503-510.
113. Karler R., Calder L.D., Turkanis S.A. Prolonged CNS hyperexcitability in mice after a single exposure to delta-9-tetrahydrocannabinol. Neuropharmacology 1986, 25:441-446.
114. Isokawa M., Alger B.E. Retrograde endocannabinoid regulation of GABAergic inhibition in the rat dentate gyrus granule cell. J Physiol 2005, 567(Pt. 3):1001-1010.
115. Bhaskaran M.D., Smith B.N. Effects of TRPV1 activation on synaptic excitation in the dentate gyrus of a mouse model of temporal lobe epilepsy. Exp Neurol 2010, 223:529-536.
116. Dragunow M. Adenosine: the brain's natural anticonvulsant?. Trends Pharmacol Sci 1986, 7:128-130.
117. Vezzani A., Sperk G. Overexpression of NPY and Y2 receptors in epileptic brain tissue: an endogenous neuroprotective mechanism in temporal lobe epilepsy?. Neuropeptides 2004, 38:245-252.
118. Boison D. Adenosine and epilepsy: from therapeutic rationale to new therapeutic strategies. Neuroscientist 2005, 11:25-36.
119. Dunwiddie T.V., Masino S.A. The role and regulation of adenosine in the central nervous system. Annu Rev Neurosci 2001, 24:31-55.
120. During M.J., Spencer D.D. Adenosine: a potential mediator of seizure arrest and postictal refractoriness. Ann Neurol 1992, 32:618-624.
121. Boison D., Stewart K.A. Therapeutic epilepsy research: from pharmacological rationale to focal adenosine augmentation. Biochem Pharmacol 2009, 78:1428-1437.
122. Boison D. The adenosine kinase hypothesis of epileptogenesis. Prog Neurobiol 2008, 84:249-262.
123. Meurs A., Clinckers R., Ebinger G., Michotte Y., Smolders I. Clinical potential of neuropeptide Y receptor ligands in the treatment of epilepsy. Curr Top Med Chem 2007, 7:1660-1674.
124. Noe F., Frasca A., Balducci C., et al. Neuropeptide Y overexpression using recombinant adeno-associated viral vectors. Neurotherapeutics 2009, 6:300-306.
125. Kaila K., Chesler M. Activity-evoked changes in extracellular pH. pH and brain function 1998, 309-330. Wiley-Liss, New York. K. Kaila, B.R. Ransom (Eds.).
126. Lennox W.G. The effect on epileptic seizures of varying the composition of the respired air. J Clin Invest 1929, 4:23-24.
127. Mitchell W.G., Grubbs R.C. Inhibition of audiogenic seizures by carbon dioxide. Science 1956, 123:223-224.
128. Woodbury D.M., Rollins L.T., Henrie J.R., Jones J.C., Sato T. Effects of carbon dioxide and oxygen on properties of experimental seizures in mice. Am J Physiol 1956, 184:202-208.
129. Tschirgi R.D., Taylor J.L. Slowly changing bioelectric potentials associated with the blood-brain barrier. Am J Physiol 1958, 195:7-22.
130. Meduna L.J. The physiological basis of carbon dioxide treatment. Carbon dioxide therapy 1958, 3-19. Charles C Thomas, Springfield, IL. L.J. Meduna (Ed.).
131. Wang R.I., Sonnenschein R.R. PH of cerebral cortex during induced convulsions. J Neurophysiol 1955, 18:130-137.