Jump to ContentJump to Main Navigation
Show Summary Details
More options …

Reviews in the Neurosciences

Editor-in-Chief: Huston, Joseph P.

Editorial Board: Topic, Bianca / Adeli, Hojjat / Buzsaki, Gyorgy / Crawley, Jacqueline / Crow, Tim / Gold, Paul / Holsboer, Florian / Korth, Carsten / Li, Jay-Shake / Lubec, Gert / McEwen, Bruce / Pan, Weihong / Pletnikov, Mikhail / Robbins, Trevor / Schnitzler, Alfons / Stevens, Charles / Steward, Oswald / Trojanowski, John


IMPACT FACTOR 2017: 2.590
5-year IMPACT FACTOR: 3.078

CiteScore 2017: 2.81

SCImago Journal Rank (SJR) 2017: 0.980
Source Normalized Impact per Paper (SNIP) 2017: 0.804

Online
ISSN
2191-0200
See all formats and pricing
More options …
Volume 26, Issue 2

Issues

Pathologic role of neuronal nicotinic acetylcholine receptors in epileptic disorders: implication for pharmacological interventions

Mehdi Ghasemi
  • Corresponding author
  • Department of Neurology, University of Massachusetts Medical School, Worcester, MA 01655, USA
  • Department of Neurology, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA
  • NeurExpand Brain Center, 1205 York Road, Lutherville, MD 21093, USA
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Arash Hadipour-Niktarash
  • Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02114, USA
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
Published Online: 2015-01-07 | DOI: https://doi.org/10.1515/revneuro-2014-0044

Abstract

Accumulating evidence suggests that neuronal nicotinic acetylcholine receptors (nAChRs) may play a key role in the pathophysiology of some neurological diseases such as epilepsy. Based on genetic studies in patients with epileptic disorders worldwide and animal models of seizure, it has been demonstrated that nAChR activity is altered in some specific types of epilepsy, including autosomal dominant nocturnal frontal lobe epilepsy (ADNFLE) and juvenile myoclonic epilepsy (JME). Neuronal nAChR antagonists also have antiepileptic effects in pre-clinical studies. There is some evidence that conventional antiepileptic drugs may affect neuronal nAChR function. In this review, we re-examine the evidence for the involvement of nAChRs in the pathophysiology of some epileptic disorders, especially ADNFLE and JME, and provide an overview of nAChR antagonists that have been evaluated in animal models of seizure.

Keywords: acetylcholine; autosomal dominant nocturnal frontal lobe epilepsy (ADNFLE); epilepsy; juvenile myoclonic epilepsy (JME); neuronal nicotinic acetylcholine receptor (nAChR); nicotinic receptor antagonist; seizure

References

  • Aceto, M.D., Bentley, H.C., and Dembinski, J.R. (1969). Effects of ganglion blocking agents on nicotine extensor convulsions and lethality in mice. Br. J. Pharmacol. 37, 104–111.Google Scholar

  • Albuquerque, E.X., Pereira, E.F., Alkondon, M., and Rogers, S.W. (2009). Mammalian nicotinic acetylcholine receptors: from structure to function. Physiol. Rev. 89, 73–120.CrossrefPubMedGoogle Scholar

  • Alkondon, M. and Albuquerque, E.X. (2004). The nicotinic acetylcholine receptor subtypes and their function in the hippocampus and cerebral cortex. Prog. Brain Res. 145, 109–120.PubMedCrossrefGoogle Scholar

  • Aracri, P., Amadeo, A., Pasini, M.E., Fascio, U., and Becchetti, A. (2013). Regulation of glutamate release by heteromeric nicotinic receptors in layer V of the secondary motor region (Fr2) in the dorsomedial shoulder of prefrontal cortex in mouse. Synapse 67, 338–357.Google Scholar

  • Aridon, P., Marini, C., Di Resta, C., Brilli, E., De Fusco, M., Politi, F., Parrini, E., Manfredi, I., Pisano, T., Pruna, D., et al. (2006). Increased sensitivity of the neuronal nicotinic receptor alpha 2 subunit causes familial epilepsy with nocturnal wandering and ictal fear. Am. J. Hum. Genet. 79, 342–350.CrossrefGoogle Scholar

  • Bagri, A., Di Scala, G., and Sandner, G. (1999). Myoclonic and tonic seizures elicited by microinjection of cholinergic drugs into the inferior colliculus. Therapie 54, 589–594.Google Scholar

  • Banerjee, S., Punzi, J.S., Kreilick, K., and Abood, L.G. (1990). [3H]mecamylamine binding to rat brain membranes. Studies with mecamylamine and nicotine analogues. Biochem. Pharmacol. 40, 2105–2110.CrossrefPubMedGoogle Scholar

  • Banerjee, J., Alkondon, M., Pereira, E.F., and Albuquerque, E.X. (2012). Regulation of GABAergic inputs to CA1 pyramidal neurons by nicotinic receptors and kynurenic acid. J. Pharmacol. Exp. Ther. 341, 500–509.Google Scholar

  • Beker, F., Weber, M., Fink, R.H., and Adams, D.J. (2003). Muscarinic and nicotinic ACh receptor activation differentially mobilize Ca2+ in rat intracardiac ganglion neurons. J. Neurophysiol. 90, 1956–1964.CrossrefGoogle Scholar

  • Beleslin, D.B. and Krstic, S.K. (1986). Nicotine-induced convulsions in cats and central nicotinic receptors. Pharmacol. Biochem. Behav. 24, 1509–1511.PubMedCrossrefGoogle Scholar

  • Berkovic, S.F., Howell, R.A., Hay, D.A., and Hopper, J.L. (1998). Epilepsies in twins: genetics of the major epilepsy syndromes. Ann. Neurol. 43, 435–445.CrossrefPubMedGoogle Scholar

  • Bertrand, D., Picard, F., Le Hellard, S., Weiland, S., Favre, I., Phillips, H., Bertrand, S., Berkovic, S.F., Malafosse, A., and Mulley, J. (2002). How mutations in the nAChRs can cause ADNFLE epilepsy. Epilepsia 43(Suppl 5), 112–122.CrossrefGoogle Scholar

  • Bialer, M. and Yagen, B. (2007). Valproic acid: second generation. Neurotherapeutics 4, 130–137.PubMedCrossrefGoogle Scholar

  • Bitner, R.S. and Nikkel, A.L. (2002). Alpha-7 nicotinic receptor expression by two distinct cell types in the dorsal raphe nucleus and locus coeruleus of rat. Brain Res. 938, 45–54.Google Scholar

  • Brain, K.L., Trout, S.J., Jackson, V.M., Dass, N., and Cunnane, T.C. (2001). Nicotine induces calcium spikes in single nerve terminal varicosities: a role for intracellular calcium stores. Neuroscience 106, 395–403.CrossrefPubMedGoogle Scholar

  • Brawek, B., Loffler, M., Dooley, D.J., Weyerbrock, A., and Feuerstein, T.J. (2008). Differential modulation of K(+)-evoked (3)H-neurotransmitter release from human neocortex by gabapentin and pregabalin. Naunyn Schmiedebergs Arch. Pharmacol. 376, 301–307.Google Scholar

  • Briggs, S.W. and Galanopoulou, A.S. (2011). Altered GABA signaling in early life epilepsies. Neural Plast. 2011, 527–605.Google Scholar

  • Burnashev, N., Zhou, Z., Neher, E., and Sakmann, B. (1995). Fractional calcium currents through recombinant GluR channels of the NMDA, AMPA and kainate receptor subtypes. J. Physiol. 485(Pt 2), 403–418.Google Scholar

  • Caulfield, M.P. and Higgins, G.A. (1983). Mediation of nicotine-induced convulsions by central nicotinic receptors of the ‘C6’ type. Neuropharmacology 22, 347–351.CrossrefGoogle Scholar

  • Champtiaux, N., Gotti, C., Cordero-Erausquin, M., David, D.J., Przybylski, C., Lena, C., Clementi, F., Moretti, M., Rossi, F.M., Le Novere, N., et al. (2003). Subunit composition of functional nicotinic receptors in dopaminergic neurons investigated with knock-out mice. J. Neurosci. 23, 7820–7829.Google Scholar

  • Chaney, L.A., Rockhold, R.W., Wineman, R.W., and Hume, A.S. (1999). Anticonvulsant-resistant seizures following pyridostigmine bromide (PB) and N,N-diethyl-m-toluamide (DEET). Toxicol. Sci. 49, 306–311.CrossrefPubMedGoogle Scholar

  • Chang, B.S. and Lowenstein, D.H. (2003). Epilepsy. N. Engl. J. Med. 349, 1257–1266.Google Scholar

  • Chaturvedi, A.K. (1984). Effects of mecamylamine, nicotine, atropine and physostigmine on the phencyclidine-induced behavioral toxicity. Pharmacol. Biochem. Behav. 20, 559–566.CrossrefPubMedGoogle Scholar

  • Chen, Y., Wu, L., Fang, Y., He, Z., Peng, B., Shen, Y., and Xu, Q. (2009). A novel mutation of the nicotinic acetylcholine receptor gene CHRNA4 in sporadic nocturnal frontal lobe epilepsy. Epilepsy Res. 83, 152–156.CrossrefGoogle Scholar

  • Cheng, L.Z., Han, L., Fan, J., Huang, L.T., Peng, L.C., and Wang, Y. (2011). Enhanced inhibitory synaptic transmission in the spinal dorsal horn mediates antinociceptive effects of TC-2559. Mol. Pain 7, 56.PubMedCrossrefGoogle Scholar

  • Chioza, B., Goodwin, H., Blower, J., McCormick, D., Nashef, L., Asherson, P., and Makoff, A.J. (2000). Failure to replicate association between the gene for the neuronal nicotinic acetylcholine receptor alpha 4 subunit (CHRNA4) and IGE. Am. J. Med. Genet. 96, 814–816.CrossrefGoogle Scholar

  • Cho, Y.W., Motamedi, G.K., Laufenberg, I., Sohn, S.I., Lim, J.G., Lee, H., Yi, S.D., Lee, J.H., Kim, D.K., Reba, R., et al. (2003). A Korean kindred with autosomal dominant nocturnal frontal lobe epilepsy and mental retardation. Arch. Neurol. 60, 1625–1632.CrossrefPubMedGoogle Scholar

  • Cho, Y.W., Yi, S.D., Lim, J.G., Kim, D.K., and Motamedi, G.K. (2008). Autosomal dominant nocturnal frontal lobe epilepsy and mild memory impairment associated with CHRNB2 mutation I312M in the neuronal nicotinic acetylcholine receptor. Epilepsy Behav. 13, 361–365.Google Scholar

  • Collins, A.C., Evans, C.B., Miner, L.L., and Marks, M.J. (1986). Mecamylamine blockade of nicotine responses: evidence for two brain nicotinic receptors. Pharmacol. Biochem. Behav. 24, 1767–1773.PubMedCrossrefGoogle Scholar

  • Combi, R., Dalpra, L., Tenchini, M.L., and Ferini-Strambi, L. (2004). Autosomal dominant nocturnal frontal lobe epilepsy – a critical overview. J. Neurol. 251, 923–934.Google Scholar

  • Commons, K.G. (2008). Alpha4 containing nicotinic receptors are positioned to mediate postsynaptic effects on 5-HT neurons in the rat dorsal raphe nucleus. Neuroscience 153, 851–859.CrossrefGoogle Scholar

  • Conroy, W.G. and Berg, D.K. (1998). Nicotinic receptor subtypes in the developing chick brain: appearance of a species containing the alpha4, beta2, and alpha5 gene products. Mol. Pharmacol. 53, 392–401.Google Scholar

  • Consolo, S., Bianchi, S., and Ladinsky, H. (1976). Effect of carbamazepine on cholinergic parameters in rat brain areas. Neuropharmacology 15, 653–657.CrossrefPubMedGoogle Scholar

  • Cossette, P., Liu, L., Brisebois, K., Dong, H., Lortie, A., Vanasse, M., Saint-Hilaire, J.M., Carmant, L., Verner, A., Lu, W.Y., et al. (2002). Mutation of GABRA1 in an autosomal dominant form of juvenile myoclonic epilepsy. Nat. Genet. 31, 184–189.CrossrefGoogle Scholar

  • Courtney, K.R. and Etter, E.F. (1983). Modulated anticonvulsant block of sodium channels in nerve and muscle. Eur. J. Pharmacol. 88, 1–9.PubMedCrossrefGoogle Scholar

  • Dajas-Bailador, F.A., Mogg, A.J., and Wonnacott, S. (2002). Intracellular Ca2+ signals evoked by stimulation of nicotinic acetylcholine receptors in SH-SY5Y cells: contribution of voltage-operated Ca2+ channels and Ca2+ stores. J. Neurochem. 81, 606–614.CrossrefGoogle Scholar

  • Damaj, M.I., Glassco, W., Dukat, M., and Martin, B.R. (1999). Pharmacological characterization of nicotine-induced seizures in mice. J. Pharmacol. Exp. Ther. 291, 1284–1291.Google Scholar

  • Damaj, M.I., Fonck, C., Marks, M.J., Deshpande, P., Labarca, C., Lester, H.A., Collins, A.C., and Martin, B.R. (2007). Genetic approaches identify differential roles for alpha4beta2* nicotinic receptors in acute models of antinociception in mice. J. Pharmacol. Exp. Ther. 321, 1161–1169.Google Scholar

  • Dani, J.A. and Bertrand, D. (2007). Nicotinic acetylcholine receptors and nicotinic cholinergic mechanisms of the central nervous system. Annu. Rev. Pharmacol. Toxicol. 47, 699–729.PubMedCrossrefGoogle Scholar

  • Danober, L., Depaulis, A., Marescaux, C., and Vergnes, M. (1993). Effects of cholinergic drugs on genetic absence seizures in rats. Eur. J. Pharmacol. 234, 263–268.Google Scholar

  • de Boer, T., Stoof, J.C., and van Duijn, H. (1982). The effects of convulsant and anticonvulsant drugs on the release of radiolabeled GABA, glutamate, noradrenaline, serotonin and acetylcholine from rat cortical slices. Brain Res. 253, 153–160.Google Scholar

  • De Fusco, M., Becchetti, A., Patrignani, A., Annesi, G., Gambardella, A., Quattrone, A., Ballabio, A., Wanke, E., and Casari, G. (2000). The nicotinic receptor beta 2 subunit is mutant in nocturnal frontal lobe epilepsy. Nat. Genet. 26, 275–276.Google Scholar

  • de Jong, R.H., Gamble, C.A., and Bonin, J.D. (1981). Neuromuscular blocking agents do not alter local anesthetic seizure thresholds. Exp. Neurol. 74, 628–631.CrossrefGoogle Scholar

  • Delucchi, G.A. and Calabrese, J.R. (1989). Anticonvulsants for treatment of manic depression. Cleveland Clin. J. Med. 56, 756–761.Google Scholar

  • Deutsch, S.I., Rosse, R.B., Bellack, A.S., Billingslea, E.N., and Mastropaolo, J. (2003). Methyllycaconitine fails to inhibit electrically precipitated tonic hindlimb extension in mice. Clin. Neuropharmacol. 26, 62–64.PubMedCrossrefGoogle Scholar

  • Di Resta, C., Ambrosi, P., Curia, G., and Becchetti, A. (2010). Effect of carbamazepine and oxcarbazepine on wild-type and mutant neuronal nicotinic acetylcholine receptors linked to nocturnal frontal lobe epilepsy. Eur. J. Pharmacol. 643, 13–20.Google Scholar

  • Diaz-Otero, F., Quesada, M., Morales-Corraliza, J., Martinez-Parra, C., Gomez-Garre, P., and Serratosa, J.M. (2008). Autosomal dominant nocturnal frontal lobe epilepsy with a mutation in the CHRNB2 gene. Epilepsia 49, 516–520.Google Scholar

  • Dobelis, P., Hutton, S., Lu, Y., and Collins, A.C. (2003). GABAergic systems modulate nicotinic receptor-mediated seizures in mice. J. Pharmacol. Exp. Ther. 306, 1159–1166.Google Scholar

  • Durner, M., Shinnar, S., Resor, S.R., Moshe, S.L., Rosenbaum, D., Cohen, J., Harden, C., Kang, H., Hertz, S., Wallace, S., et al. (2000). No evidence for a major susceptibility locus for juvenile myoclonic epilepsy on chromosome 15q. Am. J. Med. Genet. 96, 49–52.CrossrefGoogle Scholar

  • Eberhard, D.A. and Holz, R.W. (1987). Cholinergic stimulation of inositol phosphate formation in bovine adrenal chromaffin cells: distinct nicotinic and muscarinic mechanisms. J. Neurochem. 49, 1634–1643.CrossrefGoogle Scholar

  • Elmslie, F.V., Rees, M., Williamson, M.P., Kerr, M., Kjeldsen, M.J., Pang, K.A., Sundqvist, A., Friis, M.L., Chadwick, D., Richens, A., et al. (1997). Genetic mapping of a major susceptibility locus for juvenile myoclonic epilepsy on chromosome 15q. Hum. Mol. Genet. 6, 1329–1334.CrossrefGoogle Scholar

  • Ferini-Strambi, L., Sansoni, V., and Combi, R. (2012). Nocturnal frontal lobe epilepsy and the acetylcholine receptor. Neurologist 18, 343–349.CrossrefGoogle Scholar

  • Flores, C.M., Rogers, S.W., Pabreza, L.A., Wolfe, B.B., and Kellar, K.J. (1992). A subtype of nicotinic cholinergic receptor in rat brain is composed of alpha 4 and beta 2 subunits and is up-regulated by chronic nicotine treatment. Mol. Pharmacol. 41, 31–37.Google Scholar

  • Fucile, S. (2004). Ca2+ permeability of nicotinic acetylcholine receptors. Cell Calcium 35, 1–8.PubMedCrossrefGoogle Scholar

  • Fucile, S., Renzi, M., Lax, P., and Eusebi, F. (2003). Fractional Ca2+ current through human neuronal alpha7 nicotinic acetylcholine receptors. Cell Calcium 34, 205–209.Google Scholar

  • Futatsugi, Y. and Riviello, J.J., Jr. (1998). Mechanisms of generalized absence epilepsy. Brain Dev. 20, 75–79.PubMedCrossrefGoogle Scholar

  • Gambardella, A., Annesi, G., De Fusco, M., Patrignani, A., Aguglia, U., Annesi, F., Pasqua, A.A., Spadafora, P., Oliveri, R.L., Valentino, P., et al. (2000). A new locus for autosomal dominant nocturnal frontal lobe epilepsy maps to chromosome 1. Neurology 55, 1467–1471.Google Scholar

  • Gao, Z.G., Cui, W.Y., Liu, B.Y., Liu, C.G., and Wang, L. (1997). Anticholinergic activity in mice and receptor-binding properties in rats of a series of synthetic tropane derivatives. J. Pharm. Pharmacol. 49, 315–318.CrossrefGoogle Scholar

  • Gardner, C.R. and Webster, R.A. (1977). Convulsant-anticonvulsant interactions on seizure activity and cortical acetylcholine release. Eur. J. Pharmacol. 42, 247–256.CrossrefPubMedGoogle Scholar

  • Gerzanich, V., Wang, F., Kuryatov, A., and Lindstrom, J. (1998). Alpha 5 subunit alters desensitization, pharmacology, Ca++ permeability and Ca++ modulation of human neuronal alpha 3 nicotinic receptors. J. Pharmacol. Exp. Ther. 286, 311–320.Google Scholar

  • Ghasemi, M. and Schachter, S.C. (2011). The NMDA receptor complex as a therapeutic target in epilepsy: a review. Epilepsy Behav. 22, 617–640.PubMedCrossrefGoogle Scholar

  • Gil, Z., Sack, R.A., Kedmi, M., Harmelin, A., and Orr-Urtreger, A. (2002). Increased sensitivity to nicotine-induced seizures in mice heterozygous for the L250T mutation in the alpha7 nicotinic acetylcholine receptor. Neuroreport 13, 191–196.Google Scholar

  • Gmiro, V.E., Serdyuk, S.E., and Efremov, O.M. (2008). Peripheral and central routes of administration of quaternary ammonium compound IEM-1460 are equally potent in reducing the severity of nicotine-induced seizures in mice. Bull. Exp. Biol. Med. 146, 18–21.PubMedCrossrefGoogle Scholar

  • Gotti, C. and Clementi, F. (2004). Neuronal nicotinic receptors: from structure to pathology. Prog. Neurobiol. 74, 363–396.PubMedCrossrefGoogle Scholar

  • Gotti, C., Moretti, M., Zanardi, A., Gaimarri, A., Champtiaux, N., Changeux, J.P., Whiteaker, P., Marks, M.J., Clementi, F., and Zoli, M. (2005). Heterogeneity and selective targeting of neuronal nicotinic acetylcholine receptor (nAChR) subtypes expressed on retinal afferents of the superior colliculus and lateral geniculate nucleus: identification of a new native nAChR subtype alpha3beta2(alpha5 or beta3) enriched in retinocollicular afferents. Mol. Pharmacol. 68, 1162–1171.Google Scholar

  • Gotti, C., Moretti, M., Bohr, I., Ziabreva, I., Vailati, S., Longhi, R., Riganti, L., Gaimarri, A., McKeith, I.G., Perry, R.H., et al. (2006a). Selective nicotinic acetylcholine receptor subunit deficits identified in Alzheimer’s disease, Parkinson’s disease and dementia with Lewy bodies by immunoprecipitation. Neurobiol. Dis. 23, 481–489.CrossrefPubMedGoogle Scholar

  • Gotti, C., Zoli, M., and Clementi, F. (2006b). Brain nicotinic acetylcholine receptors: native subtypes and their relevance. Trends Pharmacol. Sci. 27, 482–491.PubMedCrossrefGoogle Scholar

  • Gotti, C., Moretti, M., Meinerz, N.M., Clementi, F., Gaimarri, A., Collins, A.C., and Marks, M.J. (2008). Partial deletion of the nicotinic cholinergic receptor alpha 4 or beta 2 subunit genes changes the acetylcholine sensitivity of receptor-mediated 86Rb+ efflux in cortex and thalamus and alters relative expression of alpha 4 and beta 2 subunits. Mol. Pharmacol. 73, 1796–1807.CrossrefPubMedGoogle Scholar

  • Gozzi, A., Schwarz, A., Reese, T., Bertani, S., Crestan, V., and Bifone, A. (2006). Region-specific effects of nicotine on brain activity: a pharmacological MRI study in the drug-naive rat. Neuropsychopharmacology 31, 1690–1703.CrossrefPubMedGoogle Scholar

  • Grady, S.R., Moretti, M., Zoli, M., Marks, M.J., Zanardi, A., Pucci, L., Clementi, F., and Gotti, C. (2009). Rodent habenulo-interpeduncular pathway expresses a large variety of uncommon nAChR subtypes, but only the alpha3beta4* and alpha3beta3beta4* subtypes mediate acetylcholine release. J. Neurosci. 29, 2272–2282.CrossrefGoogle Scholar

  • Granger, P., Biton, B., Faure, C., Vige, X., Depoortere, H., Graham, D., Langer, S.Z., Scatton, B., and Avenet, P. (1995). Modulation of the gamma-aminobutyric acid type A receptor by the antiepileptic drugs carbamazepine and phenytoin. Mol. Pharmacol. 47, 1189–1196.PubMedGoogle Scholar

  • Gray, R., Rajan, A.S., Radcliffe, K.A., Yakehiro, M., and Dani, J.A. (1996). Hippocampal synaptic transmission enhanced by low concentrations of nicotine. Nature 383, 713–716.PubMedCrossrefGoogle Scholar

  • Grinevich, V.P., Letchworth, S.R., Lindenberger, K.A., Menager, J., Mary, V., Sadieva, K.A., Buhlman, L.M., Bohme, G.A., Pradier, L., Benavides, J., et al. (2005). Heterologous expression of human {alpha}6{beta}4{beta}3{alpha}5 nicotinic acetylcholine receptors: binding properties consistent with their natural expression require quaternary subunit assembly including the {alpha}5 subunit. J. Pharmacol. Exp. Ther. 312, 619–626.Google Scholar

  • Gueorguiev, V.D., Zeman, R.J., Meyer, E.M., and Sabban, E.L. (2000). Involvement of alpha7 nicotinic acetylcholine receptors in activation of tyrosine hydroxylase and dopamine beta-hydroxylase gene expression in PC12 cells. J. Neurochem. 75, 1997–2005.Google Scholar

  • Haider, M.Z., Habeeb, Y., Al-Nakkas, E., Al-Anzi, H., Zaki, M., Al-Tawari, A., and Al-Bloushi, M. (2005). Lack of an association between candidate gene loci and idiopathic generalized epilepsy in Kuwaiti Arab children. J. Biomed. Sci. 12, 815–818.Google Scholar

  • Han, Z.Y., Le Novere, N., Zoli, M., Hill, J.A., Jr., Champtiaux, N., and Changeux, J.P. (2000). Localization of nAChR subunit mRNAs in the brain of Macaca mulatta. Eur. J. Neurosci. 12, 3664–3674.CrossrefGoogle Scholar

  • Harrison, P.K., Sheridan, R.D., Green, A.C., Scott, I.R., and Tattersall, J.E. (2004). A guinea pig hippocampal slice model of organophosphate-induced seizure activity. J. Pharmacol. Exp. Ther. 310, 678–686.CrossrefGoogle Scholar

  • Hayman, M., Scheffer, I.E., Chinvarun, Y., Berlangieri, S.U., and Berkovic, S.F. (1997). Autosomal dominant nocturnal frontal lobe epilepsy: demonstration of focal frontal onset and intrafamilial variation. Neurology 49, 969–975.PubMedCrossrefGoogle Scholar

  • Helbig, I. and Lowenstein, D.H. (2013). Genetics of the epilepsies: where are we and where are we going? Curr. Opin. Neurol. 26, 179–185.PubMedCrossrefGoogle Scholar

  • Hernandez, S.C., Vicini, S., Xiao, Y., Davila-Garcia, M.I., Yasuda, R.P., Wolfe, B.B., and Kellar, K.J. (2004). The nicotinic receptor in the rat pineal gland is an alpha3beta4 subtype. Mol. Pharmacol. 66, 978–987.CrossrefGoogle Scholar

  • Hill, J.A., Jr., Zoli, M., Bourgeois, J.P., and Changeux, J.P. (1993). Immunocytochemical localization of a neuronal nicotinic receptor: the beta 2-subunit. J. Neurosci. 13, 1551–1568.Google Scholar

  • Hillmer, A.T., Wooten, D.W., Moirano, J.M., Slesarev, M., Barnhart, T.E., Engle, J.W., Nickles, R.J., Murali, D., Schneider, M.L., Mukherjee, J., et al. (2011). Specific alpha4beta2 nicotinic acetylcholine receptor binding of [F-18]nifene in the rhesus monkey. Synapse 65, 1309–1318.Google Scholar

  • Hirose, S., Iwata, H., Akiyoshi, H., Kobayashi, K., Ito, M., Wada, K., Kaneko, S., and Mitsudome, A. (1999). A novel mutation of CHRNA4 responsible for autosomal dominant nocturnal frontal lobe epilepsy. Neurology 53, 1749–1753.Google Scholar

  • Hoda, J.C., Gu, W., Friedli, M., Phillips, H.A., Bertrand, S., Antonarakis, S.E., Goudie, D., Roberts, R., Scheffer, I.E., Marini, C., et al. (2008). Human nocturnal frontal lobe epilepsy: pharmocogenomic profiles of pathogenic nicotinic acetylcholine receptor beta-subunit mutations outside the ion channel pore. Mol. Pharmacol. 74, 379–391.CrossrefPubMedGoogle Scholar

  • Holder, J.L. Jr. and Wilfong, A.A. (2011). Zonisamide in the treatment of epilepsy. Expert Opin. Pharmacother. 12, 2573–2581.Google Scholar

  • Huang, M., Li, Z., Ichikawa, J., Dai, J., and Meltzer, H.Y. (2006). Effects of divalproex and atypical antipsychotic drugs on dopamine and acetylcholine efflux in rat hippocampus and prefrontal cortex. Brain Res. 1099, 44–55.Google Scholar

  • Huguenard, J.R. and McCormick, D.A. (2007). Thalamic synchrony and dynamic regulation of global forebrain oscillations. Trends Neurosci. 30, 350–356.CrossrefPubMedGoogle Scholar

  • Hunter, B.E., de Fiebre, C.M., Papke, R.L., Kem, W.R., and Meyer, E.M. (1994). A novel nicotinic agonist facilitates induction of long-term potentiation in the rat hippocampus. Neurosci. Lett. 168, 130–134.PubMedCrossrefGoogle Scholar

  • Ishii, K., Wong, J.K., and Sumikawa, K. (2005). Comparison of alpha2 nicotinic acetylcholine receptor subunit mRNA expression in the central nervous system of rats and mice. J. Comp. Neurol. 493, 241–260.Google Scholar

  • Itier, V. and Bertrand, D. (2001). Neuronal nicotinic receptors: from protein structure to function. FEBS Lett. 504, 118–125.Google Scholar

  • Itier, V. and Bertrand, D. (2002). Mutations of the neuronal nicotinic acetylcholine receptors and their association with ADNFLE. Neurophysiol. Clin. 32, 99–107.CrossrefPubMedGoogle Scholar

  • Ito, M., Kobayashi, K., Fujii, T., Okuno, T., Hirose, S., Iwata, H., Mitsudome, A., and Kaneko, S. (2000). Electroclinical picture of autosomal dominant nocturnal frontal lobe epilepsy in a Japanese family. Epilepsia 41, 52–58.CrossrefGoogle Scholar

  • Ivy Carroll, F., Ma, W., Navarro, H.A., Abraham, P., Wolckenhauer, S.A., Damaj, M.I., and Martin, B.R. (2007). Synthesis, nicotinic acetylcholine receptor binding, antinociceptive and seizure properties of methyllycaconitine analogs. Bioorg. Med. Chem. 15, 678–685.CrossrefGoogle Scholar

  • Jones, E.G. (2010). Chapter 7: The Thalamus. Handbook of Brain Microcircuits. G.M. Shepherd and S. Grillner, eds. (New York: Oxford University Press), pp. 59–75.Google Scholar

  • Kendziorra, K., Wolf, H., Meyer, P.M., Barthel, H., Hesse, S., Becker, G.A., Luthardt, J., Schildan, A., Patt, M., Sorger, D., et al. (2011). Decreased cerebral alpha4beta2* nicotinic acetylcholine receptor availability in patients with mild cognitive impairment and Alzheimer’s disease assessed with positron emission tomography. Eur. J. Nucl. Med. Mol. Imaging 38, 515–525.CrossrefGoogle Scholar

  • Klink, R., de Kerchove d’Exaerde, A., Zoli, M., and Changeux, J.P. (2001). Molecular and physiological diversity of nicotinic acetylcholine receptors in the midbrain dopaminergic nuclei. J. Neurosci. 21, 1452–1463.Google Scholar

  • Kulak, J.M. and Schneider, J.S. (2004). Differences in alpha7 nicotinic acetylcholine receptor binding in motor symptomatic and asymptomatic MPTP-treated monkeys. Brain Res. 999, 193–202.Google Scholar

  • Kurahashi, H. and Hirose, S. (1993). Autosomal Dominant Nocturnal Frontal Lobe Epilepsy. In GeneReviews(R). Pagon, R.A., Adam, M.P., Ardinger, H.H., Bird, T.D., Dolan, C.R., Fong, C.T., Smith, R.J.H., Stephens, K., eds. (Seattle, WA: University of Washington).PubMedGoogle Scholar

  • Kuryatov, A., Gerzanich, V., Nelson, M., Olale, F., and Lindstrom, J. (1997). Mutation causing autosomal dominant nocturnal frontal lobe epilepsy alters Ca2+ permeability, conductance, and gating of human alpha4beta2 nicotinic acetylcholine receptors. J. Neurosci. 17, 9035–9047.Google Scholar

  • Kwan, P., Schachter, S.C., and Brodie, M.J. (2011). Drug-resistant epilepsy. N. Engl. J. Med. 365, 919–926.Google Scholar

  • Labate, A., Mumoli, L., Fratto, A., Quattrone, A., and Gambardella, A. (2013). Hippocampal sclerosis worsens autosomal dominant nocturnal frontal lobe epilepsy (ADNFLE) phenotype related to CHRNB2 mutation. Eur. J. Neurol. 20, 591–593.CrossrefGoogle Scholar

  • Lambe, E.K., Picciotto, M.R., and Aghajanian, G.K. (2003). Nicotine induces glutamate release from thalamocortical terminals in prefrontal cortex. Neuropsychopharmacology 28, 216–225.CrossrefPubMedGoogle Scholar

  • Leach, M.J., Baxter, M.G., and Critchley, M.A.E. (1991). Neurochemical and behavioral aspects of lamotrigine. Epilepsia 32, S4–S8.PubMedCrossrefGoogle Scholar

  • Lee, C.C., Chou, I.C., Tsai, C.H., Wan, L., Shu, Y.A., Tsai, Y., Li, T.C., and Tsai, F.J. (2007). Association of idiopathic generalized epilepsy with polymorphisms in the neuronal nicotinic acetylcholine receptor subunits. J. Clin. Lab. Anal. 21, 67–70.CrossrefGoogle Scholar

  • Lena, C., Changeux, J.P., and Mulle, C. (1993). Evidence for ‘preterminal’ nicotinic receptors on GABAergic axons in the rat interpeduncular nucleus. J. Neurosci. 13, 2680–2688.Google Scholar

  • Lena, C., de Kerchove D’Exaerde, A., Cordero-Erausquin, M., Le Novere, N., del Mar Arroyo-Jimenez, M., and Changeux, J.P. (1999). Diversity and distribution of nicotinic acetylcholine receptors in the locus ceruleus neurons. Proc. Natl. Acad. Sci. USA 96, 12126–12131.CrossrefGoogle Scholar

  • Leniger, T., Kananura, C., Hufnagel, A., Bertrand, S., Bertrand, D., and Steinlein, O.K. (2003). A new Chrna4 mutation with low penetrance in nocturnal frontal lobe epilepsy. Epilepsia 44, 981–985.Google Scholar

  • Lindstrom, J. (2000). The Structures of Neuronal Nicotinic Receptors. Handbook of Experimental Pharmacology. F. Clementi, et al., eds. (New York: Springer), pp. 101–162.Google Scholar

  • Liu, H., Lu, C., Li, Z., Zhou, S., Li, X., Ji, L., Lu, Q., Lv, R., Wu, L., and Ma, X. (2011). The identification of a novel mutation of nicotinic acetylcholine receptor gene CHRNB2 in a Chinese patient: its possible implication in non-familial nocturnal frontal lobe epilepsy. Epilepsy Res. 95, 94–99.CrossrefGoogle Scholar

  • Lizasoain, I., Knowles, R.G., and Moncada, S. (1995). Inhibition by lamotrigine of the generation of nitric oxide in rat forebrain slices. J. Neurochem. 64, 636–642.Google Scholar

  • Magnusson, A., Stordal, E., Brodtkorb, E., and Steinlein, O. (2003). Schizophrenia, psychotic illness and other psychiatric symptoms in families with autosomal dominant nocturnal frontal lobe epilepsy caused by different mutations. Psychiatr. Genet. 13, 91–95.CrossrefPubMedGoogle Scholar

  • Mann, E.O. and Mody, I. (2008). The multifaceted role of inhibition in epilepsy: seizure-genesis through excessive GABAergic inhibition in autosomal dominant nocturnal frontal lobe epilepsy. Curr. Opin. Neurol. 21, 155–160.CrossrefPubMedGoogle Scholar

  • Mantegazza, M., Curia, G., Biagini, G., Ragsdale, D.S., and Avoli, M. (2010). Voltage-gated sodium channels as therapeutic targets in epilepsy and other neurological disorders. Lancet Neurol. 9, 413–424.PubMedCrossrefGoogle Scholar

  • Maton, B., Vergnes, M., Hirsch, E., and Marescaux, C. (1997). Involvement of proprioceptive feedback in brainstem-triggered convulsions. Epilepsia 38, 509–515.PubMedCrossrefGoogle Scholar

  • McCormick, D.A. and Contreras, D. (2001). On the cellular and network bases of epileptic seizures. Ann. Rev. Physiol. 63, 815–846.CrossrefGoogle Scholar

  • McCown, T.J. and Breese, G.R. (1990). Effects of apamin and nicotinic acetylcholine receptor antagonists on inferior collicular seizures. Eur. J. Pharmacol. 187, 49–58.Google Scholar

  • McIntosh, J.M., Yoshikami, D., Mahe, E., Nielsen, D.B., Rivier, J.E., Gray, W.R., and Olivera, B.M. (1994). A nicotinic acetylcholine receptor ligand of unique specificity, alpha-conotoxin ImI. J. Biol. Chem. 269, 16733–16739.Google Scholar

  • McLean, M.J. and Macdonald, R.L. (1986). Carbamazepine and 10,11-epoxycarbamazepine produce use- and voltage-dependent limitation of rapidly firing action potentials of mouse central neurons in cell culture. J. Pharmacol. Exp. Ther. 238, 727–738.Google Scholar

  • McLellan, A., Phillips, H.A., Rittey, C., Kirkpatrick, M., Mulley, J.C., Goudie, D., Stephenson, J.B., Tolmie, J., Scheffer, I.E., Berkovic, S.F., et al. (2003). Phenotypic comparison of two Scottish families with mutations in different genes causing autosomal dominant nocturnal frontal lobe epilepsy. Epilepsia 44, 613–617.PubMedCrossrefGoogle Scholar

  • Meyer, P.M., Strecker, K., Kendziorra, K., Becker, G., Hesse, S., Woelpl, D., Hensel, A., Patt, M., Sorger, D., Wegner, F., et al. (2009). Reduced alpha4beta2*-nicotinic acetylcholine receptor binding and its relationship to mild cognitive and depressive symptoms in Parkinson disease. Arch. Gen. Psychiatr. 66, 866–877.CrossrefGoogle Scholar

  • Meyerhoff, J.L. and Bates, V.E. (1985). Combined treatment with muscarinic and nicotinic cholinergic antagonists slows development of kindled seizures. Brain Res. 339, 386–389.Google Scholar

  • Miller, J.W., Gray, B.C., and Bardgett, M.E. (1992). Characterization of cholinergic regulation of seizures by the midline thalamus. Neuropharmacology 31, 349–356.CrossrefPubMedGoogle Scholar

  • Mizuno, K. (1997). Effects of carbamazepine and zonisamide on acetylcholine levels in rat striatum. Nihon Shinkei Seishin Yakurigaku Zasshi 17, 17–23.PubMedGoogle Scholar

  • Mizuno, K., Okada, M., Murakami, T., Kamata, A., Zhu, G., Kawata, Y., Wada, K., and Kaneko, S. (2000). Effects of carbamazepine on acetylcholine release and metabolism. Epilepsy Res. 40, 187–195.PubMedCrossrefGoogle Scholar

  • Monti, B., Polazzi, E., and Contestabile, A. (2009). Biochemical, molecular and epigenetic mechanisms of valproic acid neuroprotection. Curr. Mol. Pharmacol. 2, 95–109.PubMedCrossrefGoogle Scholar

  • Moretti, M., Vailati, S., Zoli, M., Lippi, G., Riganti, L., Longhi, R., Viegi, A., Clementi, F., and Gotti, C. (2004). Nicotinic acetylcholine receptor subtypes expression during rat retina development and their regulation by visual experience. Mol. Pharmacol. 66, 85–96.CrossrefPubMedGoogle Scholar

  • Mugnaini, M., Tessari, M., Tarter, G., Merlo Pich, E., Chiamulera, C., and Bunnemann, B. (2002). Upregulation of [3H]methyllycaconitine binding sites following continuous infusion of nicotine, without changes of alpha7 or alpha6 subunit mRNA: an autoradiography and in situ hybridization study in rat brain. Eur. J. Neurosci. 16, 1633–1646.CrossrefGoogle Scholar

  • Mulle, C., Vidal, C., Benoit, P., and Changeux, J.P. (1991). Existence of different subtypes of nicotinic acetylcholine receptors in the rat habenulo-interpeduncular system. J. Neurosci. 11, 2588–2597.Google Scholar

  • Myhrer, T., Enger, S., Jonassen, M., and Aas, P. (2011). Enhanced efficacy of anticonvulsants when combined with levetiracetam in soman-exposed rats. Neurotoxicology 32, 923–930.CrossrefPubMedGoogle Scholar

  • Nashmi, R. and Lester, H.A. (2006). CNS localization of neuronal nicotinic receptors. J. Mol. Neurosci. 30, 181–184.CrossrefGoogle Scholar

  • Nelson, M.E., Kuryatov, A., Choi, C.H., Zhou, Y., and Lindstrom, J. (2003). Alternate stoichiometries of alpha4beta2 nicotinic acetylcholine receptors. Mol. Pharmacol. 63, 332–341.CrossrefGoogle Scholar

  • Newman, M.B., Manresa, J.J., Sanberg, P.R., and Shytle, R.D. (2001). Nicotine induced seizures blocked by mecamylamine and its stereoisomers. Life Sci. 69, 2583–2591.CrossrefPubMedGoogle Scholar

  • Okamoto, M., Kita, T., Okuda, H., and Nakashima, T. (1992). Tolerance to the convulsions induced by daily nicotine treatment in rats. Jpn J. Pharmacol. 59, 449–455.CrossrefPubMedGoogle Scholar

  • Oldani, A., Zucconi, M., Asselta, R., Modugno, M., Bonati, M.T., Dalpra, L., Malcovati, M., Tenchini, M.L., Smirne, S., and Ferini-Strambi, L. (1998). Autosomal dominant nocturnal frontal lobe epilepsy. A video-polysomnographic and genetic appraisal of 40 patients and delineation of the epileptic syndrome. Brain 121(Pt 2), 205–223.CrossrefGoogle Scholar

  • Parikh, V., Ji, J., Decker, M.W., and Sarter, M. (2010). Prefrontal beta2 subunit-containing and alpha7 nicotinic acetylcholine receptors differentially control glutamatergic and cholinergic signaling. J. Neurosci. 30, 3518–3530.CrossrefGoogle Scholar

  • Pauly, J.R., Stitzel, J.A., Marks, M.J., and Collins, A.C. (1989). An autoradiographic analysis of cholinergic receptors in mouse brain. Brain Res. Bull. 22, 453–459.CrossrefPubMedGoogle Scholar

  • Perry, D.C., Xiao, Y., Nguyen, H.N., Musachio, J.L., Davila-Garcia, M.I., and Kellar, K.J. (2002). Measuring nicotinic receptors with characteristics of alpha4beta2, alpha3beta2 and alpha3beta4 subtypes in rat tissues by autoradiography. J. Neurochem. 82, 468–481.Google Scholar

  • Phillips, H.A., Scheffer, I.E., Berkovic, S.F., Hollway, G.E., Sutherland, G.R., and Mulley, J.C. (1995). Localization of a gene for autosomal dominant nocturnal frontal lobe epilepsy to chromosome 20q 13.2. Nat. Genet. 10, 117–118.Google Scholar

  • Phillips, H.A., Marini, C., Scheffer, I.E., Sutherland, G.R., Mulley, J.C., and Berkovic, S.F. (2000). A de novo mutation in sporadic nocturnal frontal lobe epilepsy. Ann. Neurol. 48, 264–267.CrossrefGoogle Scholar

  • Phillips, H.A., Favre, I., Kirkpatrick, M., Zuberi, S.M., Goudie, D., Heron, S.E., Scheffer, I.E., Sutherland, G.R., Berkovic, S.F., Bertrand, D., et al. (2001). CHRNB2 is the second acetylcholine receptor subunit associated with autosomal dominant nocturnal frontal lobe epilepsy. Am. J. Hum. Genet. 68, 225–231.CrossrefGoogle Scholar

  • Picard, F., Bertrand, S., Steinlein, O.K., and Bertrand, D. (1999). Mutated nicotinic receptors responsible for autosomal dominant nocturnal frontal lobe epilepsy are more sensitive to carbamazepine. Epilepsia 40, 1198–1209.CrossrefPubMedGoogle Scholar

  • Picciotto, M.R., Higley, M.J., and Mineur, Y.S. (2012). Acetylcholine as a neuromodulator: cholinergic signaling shapes nervous system function and behavior. Neuron 76, 116–129.CrossrefPubMedGoogle Scholar

  • Pichika, R., Easwaramoorthy, B., Christian, B.T., Shi, B., Narayanan, T.K., Collins, D., and Mukherjee, J. (2011). Nicotinic alpha4beta2 receptor imaging agents. Part III. Synthesis and biological evaluation of 3-(2-(S)-azetidinylmethoxy)-5-(3′-(18)F-fluoropropyl)pyridine ((18)F-nifzetidine). Nucl. Med. Biol. 38, 1183–1192.Google Scholar

  • Pincus, J.H. and Kiss, A. (1986a). Phenytoin reduces early acetylcholine release after depolarization. Brain Res. 397, 103–107.CrossrefPubMedGoogle Scholar

  • Pincus, J.H. and Kiss, A. (1986b). Phenytoin, tetrodotoxin, and acetylcholine release. Exp. Neurol. 94, 777–781.CrossrefPubMedGoogle Scholar

  • Pincus, J.H. and Weinfeld, H.M. (1984). Acetylcholine release from synaptosomes and phenytoin action. Brain Res. 296, 313–317.CrossrefPubMedGoogle Scholar

  • Provini, F., Plazzi, G., Tinuper, P., Vandi, S., Lugaresi, E., and Montagna, P. (1999). Nocturnal frontal lobe epilepsy. A clinical and polygraphic overview of 100 consecutive cases. Brain 122(Pt 6), 1017–1031.CrossrefGoogle Scholar

  • Psarropoulou, C., Boivin, M., and Laudadio, M.A. (2003). Nicotinic effects on excitatory field potentials recorded from the immature CA3 area of rat hippocampal slices. Exp. Brain Res. 152, 353–360.CrossrefGoogle Scholar

  • Quik, M., Vailati, S., Bordia, T., Kulak, J.M., Fan, H., McIntosh, J.M., Clementi, F., and Gotti, C. (2005). Subunit composition of nicotinic receptors in monkey striatum: effect of treatments with 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine or L-DOPA. Mol. Pharmacol. 67, 32–41.Google Scholar

  • Quik, M., Campos, C., Parameswaran, N., Langston, J.W., McIntosh, J.M., and Yeluashvili, M. (2010). Chronic nicotine treatment increases nAChRs and microglial expression in monkey substantia nigra after nigrostriatal damage. J. Mol. Neurosci. 40, 105–113.CrossrefGoogle Scholar

  • Raju, G.P., Sarco, D.P., Poduri, A., Riviello, J.J., Bergin, A.M., and Takeoka, M. (2007). Oxcarbazepine in children with nocturnal frontal-lobe epilepsy. Pediatr. Neurol. 37, 345–349.PubMedCrossrefGoogle Scholar

  • Rashid, M.H., Furue, H., Yoshimura, M., and Ueda, H. (2006). Tonic inhibitory role of alpha4beta2 subtype of nicotinic acetylcholine receptors on nociceptive transmission in the spinal cord in mice. Pain 125, 125–135.CrossrefGoogle Scholar

  • Rathouz, M.M. and Berg, D.K. (1994). Synaptic-type acetylcholine receptors raise intracellular calcium levels in neurons by two mechanisms. J. Neurosci. 14, 6935–6945.Google Scholar

  • Ribeiro-DaSilva, G., Pires-Barbosa, R., Prado, J.F., and Carlini, C.R. (1989). Convulsions induced by canatoxin in rats are probably a consequence of hypoxia. Braz. J. Med. Biol. Res. 22, 877–880.Google Scholar

  • Role, L.W. and Berg, D.K. (1996). Nicotinic receptors in the development and modulation of CNS synapses. Neuron 16, 1077–1085.CrossrefPubMedGoogle Scholar

  • Romigi, A., Marciani, M.G., Placidi, F., Pisani, L.R., Izzi, F., Torelli, F., and Prosperetti, C. (2008). Oxcarbazepine in nocturnal frontal-lobe epilepsy: a further interesting report. Pediatr. Neurol. 39, 298.CrossrefPubMedGoogle Scholar

  • Rozycka, A., Skorupska, E., Kostyrko, A., and Trzeciak, W.H. (2003). Evidence for S284L mutation of the CHRNA4 in a white family with autosomal dominant nocturnal frontal lobe epilepsy. Epilepsia 44, 1113–1117.Google Scholar

  • Rozycka, A., Steinborn, B., and Trzeciak, W.H. (2009). The 1674+11C>T polymorphism of CHRNA4 is associated with juvenile myoclonic epilepsy. Seizure 18, 601–603.Google Scholar

  • Saenz, A., Galan, J., Caloustian, C., Lorenzo, F., Marquez, C., Rodriguez, N., Jimenez, M.D., Poza, J.J., Cobo, A.M., Grid, D., et al. (1999). Autosomal dominant nocturnal frontal lobe epilepsy in a Spanish family with a Ser252Phe mutation in the CHRNA4 gene. Arch. Neurol. 56, 1004–1009.Google Scholar

  • Saghazadeh, A., Mastrangelo, M., and Rezaei, N. (2014). Genetic background of febrile seizures. Rev. Neurosci. 25, 129–161.PubMedGoogle Scholar

  • Sander, T., Toliat, M.R., Heils, A., Leschik, G., Becker, C., Ruschendorf, F., Rohde, K., Mundlos, S., and Nurnberg, P. (2002). Association of the 867Asp variant of the human anion exchanger 3 gene with common subtypes of idiopathic generalized epilepsy. Epilepsy Res. 51, 249–255.Google Scholar

  • Schachter, S.C. (2009). Seizure disorders. Med. Clin. North Am. 93, 343–351, viii.CrossrefGoogle Scholar

  • Scheffer, I.E., Bhatia, K.P., Lopes-Cendes, I., Fish, D.R., Marsden, C.D., Andermann, E., Andermann, F., Desbiens, R., Keene, D., Cendes, F., et al. (1995). Autosomal dominant nocturnal frontal lobe epilepsy. A distinctive clinical disorder. Brain 118(Pt 1), 61–73.CrossrefPubMedGoogle Scholar

  • Schlicker, E., Reimann, W., and Gothert, M. (1985). Gabapentin decreases monoamine release without affecting acetylcholine release in the brain. Arzneimittelforschung 35, 1347–1349.PubMedGoogle Scholar

  • Schwarz, J.R. and Grigat, G. (1989). Phenytoin and carbamazepine: potential- and frequency-dependent block of Na currents in mammalian myelinated nerve fibers. Epilepsia 30, 286–294.PubMedCrossrefGoogle Scholar

  • Sethy, V.H. and Sage, G.P. (1992). Modulation of release of acetylcholine from the striatum by a proposed excitatory amino acid antagonist U-54494A: comparison with known antagonists, diazepam and phenytoin. Neuropharmacology 31, 111–114.CrossrefGoogle Scholar

  • Sgard, F., Charpantier, E., Barneoud, P., and Besnard, F. (1999). Nicotinic receptor subunit mRNA expression in dopaminergic neurons of the rat brain. Ann. NY Acad. Sci. 868, 633–635.CrossrefGoogle Scholar

  • Sharma, G. and Vijayaraghavan, S. (2001). Nicotinic cholinergic signaling in hippocampal astrocytes involves calcium-induced calcium release from intracellular stores. Proc. Natl. Acad. Sci. USA 98, 4148–4153.CrossrefGoogle Scholar

  • Sharma, G. and Vijayaraghavan, S. (2003). Modulation of presynaptic store calcium induces release of glutamate and postsynaptic firing. Neuron 38, 929–939.PubMedCrossrefGoogle Scholar

  • Sher, E., Chen, Y., Sharples, T.J., Broad, L.M., Benedetti, G., Zwart, R., McPhie, G.I., Pearson, K.H., Baldwinson, T., and De Filippi, G. (2004). Physiological roles of neuronal nicotinic receptor subtypes: new insights on the nicotinic modulation of neurotransmitter release, synaptic transmission and plasticity. Curr. Top. Med. Chem. 4, 283–297.CrossrefGoogle Scholar

  • Sherman, S.M. (2012). Thalamocortical interactions. Curr. Opin. Neurobiol. 22, 575–579.CrossrefPubMedGoogle Scholar

  • Shih, T.M., Koviak, T.A., and Capacio, B.R. (1991). Anticonvulsants for poisoning by the organophosphorus compound soman: pharmacological mechanisms. Neurosci. Biobehav. Rev. 15, 349–362.PubMedGoogle Scholar

  • Shih, T., McDonough, J.H., Jr., and Koplovitz, I. (1999). Anticonvulsants for soman-induced seizure activity. J. Biomed. Sci. 6, 86–96.Google Scholar

  • Shoop, R.D., Chang, K.T., Ellisman, M.H., and Berg, D.K. (2001). Synaptically driven calcium transients via nicotinic receptors on somatic spines. J. Neurosci. 21, 771–781.Google Scholar

  • Silva-Barrat, C., Velluti, J., Szente, M., Batini, C., and Champagnat, J. (2005). Exaggeration of epileptic-like patterns by nicotine receptor activation during the GABA withdrawal syndrome. Brain Res. 1042, 133–143.Google Scholar

  • Sone, D., Sugawara, T., Sakakibara, E., Tomioka, Y., Taniguchi, G., Murata, Y., Watanabe, M., and Kaneko, S. (2012). A case of autosomal dominant nocturnal frontal lobe epilepsy (ADNFLE) coexisting with pervasive developmental disorder harboring SCN1A mutation in addition to CHRNB2 mutation. Epilepsy Behav. 25, 192–195.CrossrefGoogle Scholar

  • Sparks, D.L., Beach, T.G., and Lukas, R.J. (1998). Immunohistochemical localization of nicotinic beta2 and alpha4 receptor subunits in normal human brain and individuals with Lewy body and Alzheimer’s disease: preliminary observations. Neurosci. Lett. 256, 151–154.CrossrefGoogle Scholar

  • Steinlein, O.K. (2004). Genetic mechanisms that underlie epilepsy. Nat. Rev. Neurosci. 5, 400–408.PubMedCrossrefGoogle Scholar

  • Steinlein, O.K., Mulley, J.C., Propping, P., Wallace, R.H., Phillips, H.A., Sutherland, G.R., Scheffer, I.E., and Berkovic, S.F. (1995). A missense mutation in the neuronal nicotinic acetylcholine receptor alpha 4 subunit is associated with autosomal dominant nocturnal frontal lobe epilepsy. Nat. Genet. 11, 201–203.CrossrefGoogle Scholar

  • Steinlein, O., Sander, T., Stoodt, J., Kretz, R., Janz, D., and Propping, P. (1997a). Possible association of a silent polymorphism in the neuronal nicotinic acetylcholine receptor subunit alpha4 with common idiopathic generalized epilepsies. Am. J. Med. Genet. 74, 445–449.Google Scholar

  • Steinlein, O.K., Magnusson, A., Stoodt, J., Bertrand, S., Weiland, S., Berkovic, S.F., Nakken, K.O., Propping, P., and Bertrand, D. (1997b). An insertion mutation of the CHRNA4 gene in a family with autosomal dominant nocturnal frontal lobe epilepsy. Hum. Mol. Genet. 6, 943–947.Google Scholar

  • Steinlein, O.K., Stoodt, J., Mulley, J., Berkovic, S., Scheffer, I.E., and Brodtkorb, E. (2000). Independent occurrence of the CHRNA4 Ser248Phe mutation in a Norwegian family with nocturnal frontal lobe epilepsy. Epilepsia 41, 529–535.Google Scholar

  • Steinlein, O.K., Hoda, J.C., Bertrand, S., and Bertrand, D. (2012). Mutations in familial nocturnal frontal lobe epilepsy might be associated with distinct neurological phenotypes. Seizure 21, 118–123.CrossrefPubMedGoogle Scholar

  • Steriade, M. (2006). Grouping of brain rhythms in corticothalamic systems. Neuroscience 137, 1087–1106.CrossrefPubMedGoogle Scholar

  • Tammimaki, A., Horton, W.J., and Stitzel, J.A. (2011). Recent advances in gene manipulation and nicotinic acetylcholine receptor biology. Biochem. Pharmacol. 82, 808–819.CrossrefPubMedGoogle Scholar

  • Taske, N.L., Williamson, M.P., Makoff, A., Bate, L., Curtis, D., Kerr, M., Kjeldsen, M.J., Pang, K.A., Sundqvist, A., Friis, M.L., et al. (2002). Evaluation of the positional candidate gene CHRNA7 at the juvenile myoclonic epilepsy locus (EJM2) on chromosome 15q13-14. Epilepsy Res. 49, 157–172.Google Scholar

  • Tella, S.R., Korupolu, G.R., Schindler, C.W., and Goldberg, S.R. (1992). Pathophysiological and pharmacological mechanisms of acute cocaine toxicity in conscious rats. J. Pharmacol. Exp. Ther. 262, 936–946.Google Scholar

  • Teper, Y., Whyte, D., Cahir, E., Lester, H.A., Grady, S.R., Marks, M.J., Cohen, B.N., Fonck, C., McClure-Begley, T., McIntosh, J.M., et al. (2007). Nicotine-induced dystonic arousal complex in a mouse line harboring a human autosomal-dominant nocturnal frontal lobe epilepsy mutation. J. Neurosci. 27, 10128–10142.CrossrefGoogle Scholar

  • Toyohara, J., Ishiwata, K., Sakata, M., Wu, J., Nishiyama, S., Tsukada, H., and Hashimoto, K. (2010). In vivo evaluation of alpha7 nicotinic acetylcholine receptor agonists [11C]A-582941 and [11C]A-844606 in mice and conscious monkeys. PLoS One 5, e8961.Google Scholar

  • Tsai, M.C., Chen, Y.H., and Huang, S.S. (2000). Amphetamine elicited potential changes in vertebrate and invertebrate central neurons. Acta Biol. Hung. 51, 275–286.PubMedGoogle Scholar

  • Tsoucaris-Kupfer, D., Liblau, L., Legrand, M., and Schmitt, H. (1983). Central cardiovascular action of penicillin in anaesthetized dogs and rats. Neuropharmacology 22, 903–906.CrossrefGoogle Scholar

  • Tsunashima, K., Wolkersdorfer, M., Schwarzer, C., Sperk, G., and Fischer-Colbrie, R. (1997). Limbic seizures induce neuropeptide and chromogranin mRNA expression in rat adrenal medulla. Mol. Brain Res. 51, 42–48.CrossrefGoogle Scholar

  • Tsuneki, H., Klink, R., Lena, C., Korn, H., and Changeux, J.P. (2000). Calcium mobilization elicited by two types of nicotinic acetylcholine receptors in mouse substantia nigra pars compacta. Eur. J. Neurosci. 12, 2475–2485.CrossrefPubMedGoogle Scholar

  • Turner, J.R. and Kellar, K.J. (2005). Nicotinic cholinergic receptors in the rat cerebellum: multiple heteromeric subtypes. J. Neurosci. 25, 9258–9265.CrossrefGoogle Scholar

  • Uzum, G., Bahcekapili, N., Diler, A.S., and Ziylan, Y.Z. (2004). Tolerance to pentylentetrazol-induced convulsions and protection of cerebrovascular integrity by chronic nicotine. Int. J. Neurosci. 114, 735–748.PubMedCrossrefGoogle Scholar

  • Vallés, A.S., Garbus, I., and Barrantes, F.J. (2007). Lamotrigine is an open-channel blocker of the nicotinic acetylcholine receptor. Neuroreport 18, 45–50.PubMedCrossrefGoogle Scholar

  • Vallés, A.S., Garbus, I., Antollini, S.S., and Barrantes, F.J. (2008). A novel agonist effect on the nicotinic acetylcholine receptor exerted by the anticonvulsive drug Lamotrigine. Biochim. Biophys. Acta 1778, 2395–2404.PubMedGoogle Scholar

  • Vizi, E.S. and Pasztor, E. (1981). Release of acetylcholine from isolated human cortical slices: inhibitory effect of norepinephrine and phenytoin. Exp. Neurol. 73, 144–153.CrossrefPubMedGoogle Scholar

  • Wada, E., McKinnon, D., Heinemann, S., Patrick, J., and Swanson, L.W. (1990). The distribution of mRNA encoded by a new member of the neuronal nicotinic acetylcholine receptor gene family (alpha 5) in the rat central nervous system. Brain Res. 526, 45–53.Google Scholar

  • Waldmeier, P.C., Baumann, P.A., Wicki, P., Feldtrauer, J.J., Stierlin, C., and Schmutz, M. (1995). Similar potency of carbamazepine, oxcarbazepine, and lamotrigine in inhibiting the release of glutamate and other neurotransmitters. Neurology 45, 1907–1913.CrossrefPubMedGoogle Scholar

  • Wallace, T.L. and Porter, R.H. (2011). Targeting the nicotinic alpha7 acetylcholine receptor to enhance cognition in disease. Biochem. Pharmacol. 82, 891–903.CrossrefGoogle Scholar

  • Wang, M.Y., Liu, X.Z., Wang, J., Luan, G.M., and Wu, L.W. (2014). A novel mutation of the nicotinic acetylcholine receptor gene CHRNA4 in a Chinese patient with non-familial nocturnal frontal lobe epilepsy. Epilepsy Res. Sep 16.CrossrefGoogle Scholar

  • Willow, M., Kuenzel, E.A., and Catterall, W.A. (1984). Inhibition of voltage-sensitive sodium channels in neuroblastoma cells and synaptosomes by the anticonvulsant drugs diphenylhydantoin and carbamazepine. Mol. Pharmacol. 25, 228–234.PubMedGoogle Scholar

  • Wonnacott, S. (1997). Presynaptic nicotinic ACh receptors. Trends Neurosci. 20, 92–98.PubMedCrossrefGoogle Scholar

  • Yakel, J.L. (2012). Nicotinic ACh receptors in the hippocampus: role in excitability and plasticity. Nicotine Tob. Res. 14, 1249–1257.CrossrefGoogle Scholar

  • Yamamoto, R., Yanagita, T., Kobayashi, H., Yokoo, H., and Wada, A. (1997). Up-regulation of sodium channel subunit mRNAs and their cell surface expression by antiepileptic valproic acid: activation of calcium channel and catecholamine secretion in adrenal chromaffin cells. J. Neurochem. 68, 1655–1662.Google Scholar

  • Yang, J., McBride, S., Mak, D.O., Vardi, N., Palczewski, K., Haeseleer, F., and Foskett, J.K. (2002). Identification of a family of calcium sensors as protein ligands of inositol trisphosphate receptor Ca(2+) release channels. Proc. Natl. Acad. Sci. USA 99, 7711–7716.CrossrefGoogle Scholar

  • Young, T., Wittenauer, S., McIntosh, J.M., and Vincler, M. (2008). Spinal alpha3beta2* nicotinic acetylcholine receptors tonically inhibit the transmission of nociceptive mechanical stimuli. Brain Res. 1229, 118–124.Google Scholar

  • Zarei, M.M., Radcliffe, K.A., Chen, D., Patrick, J.W., and Dani, J.A. (1999). Distributions of nicotinic acetylcholine receptor alpha7 and beta2 subunits on cultured hippocampal neurons. Neuroscience 88, 755–764.CrossrefGoogle Scholar

  • Zheng, C., Yang, K., Liu, Q., Wang, M.Y., Shen, J., Vallés, A.S., Lukas, R.J., Barrantes, F.J., and Wu, J. (2010). The anticonvulsive drug lamotrigine blocks neuronal {alpha}4{beta}2 nicotinic acetylcholine receptors. J. Pharmacol. Exp. Ther. 335, 401–408.Google Scholar

  • Zhu, G., Okada, M., Murakami, T., Kawata, Y., Kamata, A., and Kaneko, S. (2002). Interaction between carbamazepine, zonisamide and voltage-sensitive Ca2+ channel on acetylcholine release in rat frontal cortex. Epilepsy Res. 49, 49–60.CrossrefGoogle Scholar

  • Zimmerman, G., Njunting, M., Ivens, S., Tolner, E.A., Behrens, C.J., Gross, M., Soreq, H., Heinemann, U., and Friedman, A. (2008). Acetylcholine-induced seizure-like activity and modified cholinergic gene expression in chronically epileptic rats. Eur. J. Neurosci. 27, 965–975.CrossrefPubMedGoogle Scholar

  • Zoli, M., Moretti, M., Zanardi, A., McIntosh, J.M., Clementi, F., and Gotti, C. (2002). Identification of the nicotinic receptor subtypes expressed on dopaminergic terminals in the rat striatum. J. Neurosci. 22, 8785–8789.Google Scholar

About the article

Corresponding author: Mehdi Ghasemi, Department of Neurology, University of Massachusetts Medical School, Worcester, MA 01655, USA, e-mail: ; Department of Neurology, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA; and NeurExpand Brain Center, 1205 York Road, Lutherville, MD 21093, USA


Received: 2014-06-28

Accepted: 2014-10-16

Published Online: 2015-01-07

Published in Print: 2015-04-01


Citation Information: Reviews in the Neurosciences, Volume 26, Issue 2, Pages 199–223, ISSN (Online) 2191-0200, ISSN (Print) 0334-1763, DOI: https://doi.org/10.1515/revneuro-2014-0044.

Export Citation

©2015 by De Gruyter.Get Permission

Citing Articles

Here you can find all Crossref-listed publications in which this article is cited. If you would like to receive automatic email messages as soon as this article is cited in other publications, simply activate the “Citation Alert” on the top of this page.

[1]
Dinesh C. Indurthi, Taima Qudah, Vivian W. Liao, Philip K. Ahring, Trevor M. Lewis, Thomas Balle, Mary Chebib, and Nathan L Absalom
Pharmacological Research, 2018
[2]
Yong-li Jiang, Fang Yuan, Ying Yang, Xiao-long Sun, Lu Song, and Wen Jiang
Seizure, 2018, Volume 56, Page 88
[3]
Monica Puligheddu, Miriam Melis, Giuliano Pillolla, Giulia Milioli, Liborio Parrino, Giovanni Mario Terzano, Sonia Aroni, Claudia Sagheddu, Francesco Marrosu, Marco Pistis, and Anna Lisa Muntoni
Epilepsia, 2017

Comments (0)

Please log in or register to comment.
Log in