GABAergic synchronization in epilepsy

Cold Spring Harbor Perspectives in Medicine

Volumn 6, Issue 2, 2016, Pages

  Khazipov, Roustem ^a,b,c  

^a Turing Center for Living Systems CENTURI Aix Marseille University   (France)

^b AIX MARSEILLE UNIVERSITY   (France)

^c KAZAN FEDERAL UNIVERSITY   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID B RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN; NICOTINIC RECEPTOR; 4 AMINOBUTYRIC ACID RECEPTOR; ANTICONVULSIVE AGENT; PHENOBARBITAL;

ACTION POTENTIAL; ARTICLE; AUTOSOMAL DOMINANT INHERITANCE; BRAIN CORTEX; CELL SYNCHRONIZATION; CORTICAL SYNCHRONIZATION; ELECTRIC POTENTIAL; ELECTROENCEPHALOGRAPHY; EPILEPSY; EPILEPTIC DISCHARGE; EXCITATORY POSTSYNAPTIC POTENTIAL; FRONTAL LOBE EPILEPSY; GABAERGIC SYSTEM; HIGH FREQUENCY OSCILLATION; HIPPOCAMPAL SLICE; HIPPOCAMPUS; HUMAN; INTERNEURON; LATERAL GENICULATE BODY; MEMBRANE DEPOLARIZATION; NERVE CELL NETWORK; NONHUMAN; PROTEIN BINDING; PYRAMIDAL NERVE CELL; SPIKE; SYNAPSE; ANIMAL; DISEASE MODEL; PATHOPHYSIOLOGY; PHYSIOLOGY; RAT; SYNAPTIC TRANSMISSION;

ACTION POTENTIALS; ANIMALS; ANTICONVULSANTS; CORTICAL SYNCHRONIZATION; DISEASE MODELS, ANIMAL; EPILEPSY; GAMMA-AMINOBUTYRIC ACID; HUMANS; NERVE NET; PHENOBARBITAL; RATS; RECEPTORS, GABA; SYNAPTIC TRANSMISSION;

EID: 84956684756     PISSN: None     EISSN: 21571422     Source Type: Journal    
DOI: 10.1101/cshperspect.a022764     Document Type: Article

References (78)

1. Baram TZ, Snead OC. 1990. Bicuculline induced seizures in infant rats: Ontogeny of behavioral and electrocortical phenomena. Dev Brain Res 57: 291–295.
2. Bazelot M, Dinocourt C, Cohen I, Miles R. 2010. Unitary inhibitory field potentials in the CA3 region of rat hippocampus. J Physiol 588: 2077–2090.
3. Ben-Ari Y, Cherubini E, Corradetti R, Gaïarsa JL. 1989. Giant synaptic potentials in immature rat CA3 hippocampal neurones. J Physiol 416: 303–325.
4. Ben-Ari Y, Gaiarsa JL, Tyzio R, Khazipov R. 2007. GABA: A pioneer transmitter that excites immature neurons and generates primitive oscillations. Physiol Rev 87: 1215–1284.
5. Beyeler A, Retailleau A, Molter C, Mehidi A, Szabadics J, Leinekugel X. 2013. Recruitment of perisomatic inhibition during spontaneous hippocampal activity. PLoS ONE 8: e66509.
6. Blaesse P, Airaksinen MS, Rivera C, Kaila K. 2009. Cationchloride cotransporters and neuronal function. Neuron 61: 820–838.
7. Bolea S, Avignone E, Berretta N, Sanchez-Andres JV, Cherubini E. 1999. Glutamate controls the induction of GABA-mediated giant depolarizing potentials through AMPA receptors in neonatal rat hippocampal slices. J Neurophysiol 81: 2095–2102.
8. Bonifazi P, Goldin M, Picardo MA, Jorquera I, Cattani A, Bianconi G, Represa A, Ben-Ari Y, Cossart R. 2009. GABAergic hub neurons orchestrate synchrony in developing hippocampal networks. Science 326: 1419–1424.
9. Buzsaki G. 2006. Rhythms of the brain. Oxford University Press, New York.
10. Chen G, Trombley PQ, van den Pol AN. 1996. Excitatory actions of GABA in developing rat hypothalamic neurones. J Physiol 494: 451–464.
11. Cohen I, Navarro V, Clemenceau S, Baulac M, Miles R. 2002. On the origin of interictal activity in human temporal lobe epilepsy in vitro. Science 298: 1418–1421.
12. Connors BW. 1984. Initiation of synchronized neuronal bursting in neocortex. Nature 310: 685–687.
13. Csicsvari J, Jamieson B, Wise KD, Buzsaki G. 2003. Mechanisms of g oscillations in the hippocampus of the behaving rat. Neuron 37: 311–322.
14. Curtis DR, Felix D, McLellan H. 1970. GABA and hippocampal inhibition. Br J Pharmacol 40: 881–883.
15. Dzhala VI, Talos DM, Sdrulla DA, Brumback AC, Mathews GC, Benke TA, Delpire E, Jensen FE, Staley KJ. 2005. NKCC1 transporter facilitates seizures in the developing brain. Nat Med 11: 1205–1213.
16. Dzhala VI, Brumback AC, Staley KJ. 2008. Bumetanide enhances phenobarbital efficacy in a neonatal seizure model. Ann Neurol 63: 222–235.
17. Dzhala VI, Kuchibhotla KV, Glykys JC, Kahle KT, Swiercz WB, Feng G, Kuner T, Augustine GJ, Bacskai BJ, Staley KJ. 2010. Progressive NKCC1-dependent neuronal chloride accumulation during neonatal seizures. J Neurosci 30: 11745–11761.
18. Freund T, Buzsaki G. 1996. Interneurons of the hippocampus. Hippocampus 6: 345–470.
19. Fujiwara-Tsukamoto Y, Isomura Y, Nambu A, Takada M. 2003. Excitatory GABA input directly drives seizure-like rhythmic synchronization in mature hippocampal CA1 pyramidal cells. Neuroscience 119: 265–275.
20. Fujiwara-Tsukamoto Y, Isomura Y, Imanishi M, Ninomiya T, Tsukada M, Yanagawa Y, Fukai T, Takada M. 2010. Prototypic seizure activity driven by mature hippocampal fast-spiking interneurons. J Neurosci 30: 13679–13689.
21. Garaschuk O, Linn J, Eilers J, Konnerth A. 2000. Large-scale oscillatory calcium waves in the immature cortex. Nat Neurosci 3: 452–459.
22. Glickfeld LL, Roberts JD, Somogyi P, Scanziani M. 2009. Interneurons hyperpolarize pyramidal cells along their entire somatodendritic axis. Nat Neurosci 12: 21–23.
23. Glykys J, Dzhala V, Egawa K, Balena T, Saponjian Y, Kuchibhotla KV, Bacskai BJ, Kahle KT, Zeuthen T, Staley KJ. 2014. Local impermeant anions establish the neuronal chloride concentration. Science 343: 670–675.
24. Gulledge AT, Stuart GJ. 2003. Excitatory actions of GABA in the cortex. Neuron 37: 299–309.
25. Gulyas AI, Szabo GG, Ulbert I, Holderith N, Monyer H, Erdelyi F, Szabo G, Freund TF, Hajos N. 2010. Parvalbumin- containing fast-spiking basket cells generate the field potential oscillations induced by cholinergic receptor activation in the hippocampus. J Neurosci 30: 15134–15145.
26. Huberfeld G, Wittner L, Clemenceau S, Baulac M, Kaila K, Miles R, Rivera C. 2007. Perturbed chloride homeostasis and GABAergic signaling in human temporal lobe epilepsy. J Neurosci 27: 9866–9873.
27. Isaev D, Isaeva E, Khazipov R, Holmes GL. 2005. Anticonvulsant action of GABA in the high potassium-low magnesium model of ictogenesis in the neonatal rat hippocampus in vivo and in vitro. J Neurophysiol 94: 2987–2992.
28. Isomura Y, Fujiwara-Tsukamoto Y, Takada M. 2008. A network mechanism underlying hippocampal seizure-like synchronous oscillations. Neurosci Res 61: 227–233.
29. Javaheri S, Davis C, Rogers DH. 1993. Ionic composition of cisternal CSF in acute respiratory acidosis: Lack of effect of large dose bumetanide. J Neurochem 61: 1525–1529.
30. Kaila K, Voipio J, Paalasmaa P, Pasternack M, Deisz RA. 1993. The role of bicarbonate in GABAA receptor-mediated IPSPs of rat neocortical neurones. J Physiol 464: 273–289.
31. Khalilov I, Khazipov R, Esclapez M, Ben-Ari Y. 1997. Bicuculline induces ictal seizures in the intact hippocampus recorded in vitro. Eur J Pharmacol 319: R5–R6.
32. Khalilov I, Dzhala V, Ben-Ari Y, Khazipov R. 1999. Dual role of GABA in the neonatal rat hippocampus. Dev Neurosci 21: 310–319.
33. Khalilov I, Holmes GL, Ben-Ari Y. 2003. In vitro formation of a secondary epileptogenic mirror focus by interhippo- campal propagation of seizures. Nat Neurosci 6: 1079–1085.
34. Khalilov I, Le Van QM, Gozlan H, Ben-Ari Y. 2005. Epileptogenic actions of GABA and fast oscillations in the developing hippocampus. Neuron 48: 787–796.
35. Khazipov R, Holmes GL. 2003. Synchronization of kainateinduced epileptic activity via GABAergic inhibition in the superfused rat hippocampus in vivo. J Neurosci 23: 5337–5341.
36. Khazipov R, Leinekugel, X, Khalilov I, Gaïarsa J-L, Ben-Ari Y. 1997. Synchronization of GABAergic interneuronal network inCA3 subfield of neonatal rat hippocampal slices. J Physiol 498: 763–772.
37. Khazipov R, Esclapez M, Caillard O, Bernard C, Khalilov I, Tyzio R, Hirsch J, Dzhala V, Berger B, Ben-Ari Y. 2001. Early development of neuronal activity in the primate hippocampus in utero. J Neurosci 21: 9770–9781.
38. Khazipov R, Khalilov I, Tyzio R, Morozova E, Ben-Ari Y, Holmes GL. 2004. Developmental changes in GABAergic actions and seizure susceptibility in the rat hippocampus. Eur J Neurosci 19: 590–600.
39. Kilb W, Sinning A, Luhmann HJ. 2007. Model-specific effects of bumetanide on epileptiform activity in the in vitro intact hippocampus of the newborn mouse. Neuropharmacology 53: 524–533.
40. Klaassen A, Glykys J, Maguire J, Labarca C, Mody I, Boulter J. 2006. Seizures and enhanced cortical GABAergic inhibition in two mouse models of human autosomal-dominant nocturnal frontal lobe epilepsy. Proc Natl Acad Sci 103: 19152–19157.
41. Klausberger T, Somogyi P. 2008. Neuronal diversity and temporal dynamics: The unity of hippocampal circuit operations. Science 321: 53–57.
42. Kolbaev SN, Sharopov S, Dierkes PW, Luhmann HJ, Kilb W. 2012. Phasic GABAA-receptor activation is required to suppress epileptiform activity in the CA3 region of the immature rat hippocampus. Epilepsia 53: 888–896.
43. Leinekugel X, Medina I, Khalilov I, Ben-Ari Y, Khazipov R. 1997. Ca2þ oscillations mediated by the synergistic excitatory actions of GABAA and NMDA receptors in the neonatal hippocampus. Neuron 18: 243–255.
44. Leinekugel X, Khalilov I, Ben-Ari Y, Khazipov R. 1998. Giant depolarizing potentials: The septal pole of the hippocampus paces the activity of the developing intact septohippocampal complex in vitro. J Neurosci 18: 6349–6357.
45. Lerche H, Shah M, Beck H, Noebels J, Johnston D, Vincent A. 2013. Ion channels in genetic and acquired forms of epilepsy. J Physiol 591: 753–764.
46. Loscher W, Puskarjov M, Kaila K. 2013. Cation-chloride cotransporters NKCC1 and KCC2 as potential targets for novel antiepileptic and antiepileptogenic treatments. Neuropharmacology 69: 62–74.
47. Lu T, Trussell LO. 2001. Mixed excitatory and inhibitory GABA-mediated transmission in chick cochlear nucleus. J Physiol 535: 125–131.
48. Mann EO, Paulsen O. 2007. Role of GABAergic inhibition in hippocampal network oscillations. Trends Neurosci 30: 343–349.
49. Mann EO, Suckling JM, Hajos N, Greenfield SA, Paulsen O. 2005. Perisomatic feedback inhibition underlies cholinergically induced fast network oscillations in the rat hippocampus in vitro. Neuron 45: 105–117.
50. Marchionni I, Maccaferri G. 2009. Quantitative dynamics and spatial profile of perisomatic GABAergic input during epileptiform synchronization in the CA1 hippocampus. J Physiol 587: 5691–5708.
51. Miles R, Wong RKS. 1987. Inhibitory control of local excitatory circuits in the guinea-pig hippocampus. J Physiol 388: 611–629.
52. Minlebaev M, Khazipov R. 2011. Antiepileptic effects of endogenous b-hydroxybutyrate in suckling infant rats. Epilepsy Res 95: 100–109.
53. Monsivais P, Rubel EW. 2001. Accommodation enhances depolarizing inhibition in central neurons. J Neurosci 21: 7823–7830.
54. Nardou R, Ben-Ari Y, Khalilov I. 2009. Bumetanide, an NKCC1 antagonist, does not prevent formation of epileptogenic focus but blocks epileptic focus seizures in immature rat hippocampus. J Neurophysiol 101: 2878–2888.
55. Nardou R, Yamamoto S, Chazal G, Bhar A, Ferrand N, Dulac O, Ben-Ari Y, Khalilov I. 2011. Neuronal chloride accumulation and excitatory GABA underlie aggravation of neonatal epileptiform activities by phenobarbital. Brain 134: 987–1002.
56. Olah S, Fule M, Komlosi G, Varga C, Baldi R, Barzo P, Tamas G. 2009. Regulation of cortical microcircuits by unitary GABA-mediated volume transmission. Nature 461: 1278–1281.
57. Oren I, Hajos N, Paulsen O. 2010. Identification of the current generator underlying cholinergically induced g frequency field potential oscillations in the hippocampal CA3 region. J Physiol 588: 785–797.
58. Palma E, Amici M, Sobrero F, Spinelli G, Di AS, Ragozzino D, Mascia A, Scoppetta C, Esposito V, Miledi R, et al. 2006. Anomalous levels of Cl-transporters in the hippocampal subiculum from temporal lobe epilepsy patients make GABA excitatory. Proc Natl Acad Sci 103: 8465–8468.
59. Pavlov I, Kaila K, Kullmann DM, Miles R. 2013. Cortical inhibition, pH and cell excitability in epilepsy: What are optimal targets for antiepileptic interventions? J Physiol 591: 765–774.
60. Payne JA, Rivera C, Voipio J, Kaila K. 2003. Cation-chloride co-transporters in neuronal communication, development and trauma. Trends Neurosci 26: 199–206.
61. Rheims S, Minlebaev M, Ivanov A, Represa A, Khazipov R, Holmes GL, Ben-Ari Y, Zilberter Y. 2008. Excitatory GABA in rodent developing neocortex in vitro. J Neurophysiol 100: 609–619.
62. Rivera C, Voipio J, Payne JA, Ruusuvuori E, Lahtinen H, Lamsa K, Pirvola U, Saarma M, Kaila K. 1999. The Kþ/ Cl2 co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 397: 251–255.
63. Sipila ST, Huttu K, Voipio J, Kaila K. 2006a. Intrinsic bursting of immature CA3 pyramidal neurons and consequent giant depolarizing potentials are driven by a persistentNa current and terminated by a slow Ca-activated K current. Eur J Neurosci 23: 2330–2338.
64. Sipila ST, Schuchmann S, Voipio J, Yamada J, Kaila K. 2006b. The Na-K-Cl cotransporter (NKCC1) promotes sharp waves in the neonatal rat hippocampus. J Physiol 573: 765–773.
65. Staley KJ, Mody I. 1992. Shunting of excitatory input to dentate gyrus granule cells by a depolarizing GABAA receptor- mediated postsynaptic conductance. J Neurophysiol 68: 197–212.
66. Staley KJ, Soldo BL, Proctor WR. 1995. Ionic mechanisms of neuronal excitation by inhibitory GABAA receptors. Science 269: 977–981.
67. Steriade M, McCormick DA, Sejnowski TJ. 1993. Thalamocortical oscillations in the sleeping and aroused brain. Science 262: 679–685.
68. Tollner K, Brandt C, Topfer M, Brunhofer G, Erker T, Gabriel M, Feit PW, Lindfors J, Kaila K, Loscher W. 2014. A novel prodrug-based strategy to increase effects of bumetanide in epilepsy. Ann Neurol 75: 550–562.
69. Trevelyan AJ. 2009. The direct relationship between inhibitory currents and local field potentials. J Neurosci 29: 15299–15307.
70. Trevelyan AJ, Schevon CA. 2013. How inhibition influences seizure propagation. Neuropharmacology 69: 45–54.
71. Tyzio R, Holmes GL, Ben-Ari Y, Khazipov R. 2007. Timing of the developmental switch in GABAA mediated signalling from excitation to inhibition in CA3 rat hippocampus using gramicidin perforated patch and extracellular recordings. Epilepsia 48: 96–105.
72. Tyzio R, Minlebaev M, Rheims S, Ivanov A, Jorquera I, Holmes GL, Zilberter Y, Ben-Ari Y, Khazipov R. 2008. Postnatal changes in somatic g-aminobutyric acid signalling in the rat hippocampus. Eur J Neurosci 27: 2515–2528.
73. Valeeva G, Abdullin A, Tyzio R, Skorinkin A, Nikolski E, Ben-Ari Y, Khazipov R. 2010. Temporal coding at the immature depolarizing GABAergic synapse. Front Cell Neurosci 4.
74. Viitanen T, Ruusuvuori E, Kaila K, Voipio J. 2010. The Kþ–Cl–cotransporter KCC2 promotes GABAergic excitation in the mature rat hippocampus. J Physiol 588: 1527–1540.
75. von Krosigk M, Bal T, McCormick DA. 1993. Cellular mechanisms of a synchronized oscillation in the thalamus. Science 261: 361–364.
76. Whittington MA, Cunningham MO, LeBeau FE, Racca C, Traub RD. 2011. Multiple origins of the cortical g rhythm. Dev Neurobiol 71: 92–106.
77. Wittner L, Miles R. 2007. Factors defining a pacemaker region for synchrony in the hippocampus. J Physiol 584: 867–883.
78. Yamada J, Okabe A, Toyoda H, Kilb W, Luhmann HJ, Fukuda A. 2004. Cl-uptake promoting depolarizing GABA actions in immature rat neocortical neurones is mediated by NKCC1. J Physiol 557: 829–841.