Allosteric alpha-7 nicotinic receptor modulation and P50 sensory gating in schizophrenia: A proof-of-mechanism study

Neuropharmacology

Volumn 64, Issue , 2013, Pages 197-204

  Winterer, Georg ^a,b,c,g,h   Gallinat, Jürgen ^d   Brinkmeyer, Jürgen ^b,c,e   Musso, Francesco ^b,c,e   Kornhuber, Johannes ^f   Thuerauf, Norbert ^f   Rujescu, Dan ^g   Favis, Reyna ⁱ   Sun, Yu ⁱ   Franc, Monique A ⁱ   Ouwerkerk Mahadevan, Sivi ⁱ   Janssens, Luc ⁱ   Timmers, Maarten ⁱ   Streffer, Johannes R ⁱ  

^a UNIVERSITY OF COLOGNE   (Germany)

^b FORSCHUNGSZENTRUM JÜLICH   (Germany)

^c PHARMAIMAGE BIOMARKER SOLUTIONS GMBH   (Germany)

^d CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^e HEINRICH HEINE UNIVERSITY   (Germany)

^f UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^g UNIVERSITY OF MUNICH   (Germany)

^h Focus Clinical Drug Development GmbH   (Germany)

ⁱ JANSSEN RESEARCH AND DEVELOPMENT   (Belgium)

Author keywords

CHRNA7 gene; P50 sensory gating; Pharmacogenetics; Positive allosteric 7 nicotinic acetylcholine receptor (nAChR) modulator; Schizophrenia

Indexed keywords

AMISULPRIDE; ARIPIPRAZOLE; FLUPENTIXOL; JNJ 39393406; NEUROLEPTIC AGENT; NICOTINIC AGENT; OLANZAPINE; PIPAMPERONE; PLACEBO; QUETIAPINE; RISPERIDONE; TRAZODONE; UNCLASSIFIED DRUG; VENLAFAXINE; ZIPRASIDONE; ZOPICLONE;

ADJUVANT THERAPY; ADULT; ARTICLE; CHRNA7 GENE; CLINICAL ARTICLE; CONTROLLED STUDY; CROSSOVER PROCEDURE; DISEASE SEVERITY; DOUBLE BLIND PROCEDURE; DRUG EFFECT; DRUG EFFICACY; ELECTROENCEPHALOGRAM; EVENT RELATED POTENTIAL; GENE; GENETIC VARIABILITY; HUMAN; MALE; MISMATCH NEGATIVITY; MORNING DOSAGE; MULTICENTER STUDY; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; SCHIZOPHRENIA; SENSORY GATING;

ADULT; ALLOSTERIC REGULATION; ANTIPSYCHOTIC AGENTS; COGNITION DISORDERS; CROSS-OVER STUDIES; DIAGNOSTIC AND STATISTICAL MANUAL OF MENTAL DISORDERS; DOSE-RESPONSE RELATIONSHIP, DRUG; DOUBLE-BLIND METHOD; DRUGS, INVESTIGATIONAL; HUMANS; MALE; MIDDLE AGED; MOLECULAR TARGETED THERAPY; NICOTINIC AGONISTS; NOOTROPIC AGENTS; RECEPTORS, NICOTINIC; SCHIZOPHRENIA; SENSORY GATING; SMOKING; YOUNG ADULT;

EID: 84866369454     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2012.06.040     Document Type: Article

References (80)

1. L.E. Adler, L.D. Hoffer, J. Griffith, M.C. Waldo, and R. Freedman Normalization by nicotine of deficient auditory sensory gating in the relatives of schizophrenics Biol. Psychiatry 32 1992 607 616
2. L.E. Adler, L.D. Hoffer, A. Wiser, and R. Freedman Normalization of auditory physiology by cigarette smoking in schizophrenic patients Am. J. Psychiatry 150 1993 1856 1861
3. L.E. Adler, A. Olincy, M. Waldo, J.G. Harris, J. Griffith, K. Stevens, K. Flach, H. Nagamoto, P. Bickford, S. Leonard, and R. Freedman Schizophrenia, sensory gating, and nicotinic receptors Schizophr. Bull. 24 1998 189 202
4. H.R. Arias Positive and negative modulation of nicotinic receptors Adv. Protein Chem. Struct. Biol. 80 2010 153 203
5. H.J. Aubin, H. Rollema, T.H. Svensson, and G. Winterer Smoking, quitting, and psychiatric disease: a review Neurosci. Biobehav. Rev. 36 2012 271 284
6. M.E. Benwell, D.J. Balfour, and C.E. Birrell Desensitization of the nicotine-induced mesolimbic dopamine responses during constant infusion with nicotine Br. J. Pharmacol. 114 1995 454 460
7. D. Bertrand, A. Devillers-Thiery, F. Revah, J.L. Galzi, N. Hussy, C. Mulle, S. Bertrand, M. Ballivet, and J.P. Changeux Unconventional pharmacology of a neuronal nicotinic receptor mutated in the channel domain Proc. Natl. Acad. Sci. USA 89 1992 1261 1265
8. R.S. Bitner, W.H. Bunnelle, D.J. Anderson, C.A. Briggs, J. Buccafusco, P. Curzon, M.W. Decker, J.M. Frost, J.H. Gronlien, E. Gubbins, J. Li, J. Malysz, S. Markosyan, K. Marsh, M.D. Meyer, A.L. Nikkel, R.J. Radek, H.M. Robb, D. Timmermann, J.P. Sullivan, and M. Gopalakrishnan Broad spectrum efficacy across cognitive domains by alpha7 nicotinic acetylcholine receptor agonism correlates with activation of ERK1/2 and CREB phosphorylation pathways J. Neurosci. 27 2007 10578 10587
9. D.L. Braff, and G.A. Light Preattentional and attentional cognitive deficits as targets for treating schizophrenia Psychopharmacology (Berl) 174 2004 75 85
10. J. Brinkmeyer, A. Mobascher, F. Musso, M. Schmitz, M. Wagner, I. Frommann, G. Gründer, K.N. Spreckelmeyer, T. Wienker, A. Díaz-Lacava, D. Holler, N. Dahmen, N. Thuerauf, M. Clepce, F. Kiefer, W. de Millas, J. Gallinat, and G. Winterer P50 sensory gating and smoking in the general population Addict. Biol. 16 2011 485 498
11. D.Z. Christensen, J.D. Mikkelsen, H.H. Hansen, and M.S. Thomsen Repeated administration of alpha7 nicotinic acetylcholine receptor (nAChR) agonists, but not positive allosteric modulators, increases alpha7 nAChR levels in the brain J. Neurochem. 114 2010 1205 1216
12. S.L. Cincotta, M.S. Yorek, T.M. Moschak, S.R. Lewis, and J.S. Rodefer Selective nicotinic acetylcholine receptor agonists: potential therapies for neuropsychiatric disorders with cognitive dysfunction Curr. Opin. Investig. Drugs 9 2008 47 56
13. A.C. Collins, E. Romm, and J.M. Wehner Dissociation of the apparent relationship between nicotine tolerance and up-regulation of nicotinic receptors Brain Res. Bull. 25 1990 373 379
14. J.F. Cubells, E.H. Deoreo, P.D. Harvey, S.J. Garlow, K. Garber, M.P. Adam, and C.L. Martin Pharmaco-genetically guided treatment of recurrent rage outbursts in an adult male with 15q13.3 deletion syndrome Am. J. Med. Genet. A 155A 2011 805 810
15. J.A. Dani, K.A. Radcliffe, and V.I. Pidoplichko Variations in desensitization of nicotinic acetylcholine receptors from hippocampus and midbrain dopamine areas Eur. J. Pharmacol. 393 2000 31 38
16. A.M. de Lucas-Cerrillo, M.C. Maldifassi, F. Arnalich, J. Renart, G. Atienza, R. Serantes, J. Cruces, A. Sánchez-Pacheco, E. Andrés-Mateos, and C. Montiel Function of partially duplicated human α77 nicotinic receptor subunit CHRFAM7A gene: potential implications for the cholinergic anti-inflammatory response J. Biol. Chem. 286 2011 594 606
17. S.I. Deutsch, B.L. Schwartz, N.R. Schooler, R.B. Rosse, J. Mastropaolo, and B. Gaskins First administration of cytidine diphosphocholine and galantamine in schizophrenia: a sustained alpha7 nicotinic agonist strategy Clin. Neuropharmacol. 31 2008 34 39
18. J.R. DiFranza, and R.J. Wellman Sensitization to nicotine: how the animal literature might inform future human research Nicotine Tob. Res. 9 2007 9 20
19. R.J. Erwin, B.I. Turetsky, P. Moberg, R.C. Gur, and R.E. Gur P50 abnormalities in schizophrenia: relationship to clinical and neuropsychological indices of attention Schizophr. Res. 33 1998 157 167
20. M.B. First, R.L. Spitzer, M. Giddon, and J.B. Williams The Structured Clinical Interview for DCM-IV Axis I Disorders Research Version (SCID-1) 1996 American Psychiatric Press New York
21. R. Freedman, M. Hall, L.E. Adler, and S. Leonard Evidence in postmortem brain tissue for decreased numbers of hippocampal nicotinic receptors in schizophrenia Biol. Psychiatry 38 1995 22 33
22. R. Freedman, H. Coon, M. Myles-Worsley, A. Orr-Urtreger, A. Olincy, A. Davis, M. Polymeropoulos, J. Holik, J. Hopkins, M. Hoff, J. Rosenthal, M.C. Waldo, F. Reimherr, P. Wender, J. Yaw, D.A. Young, C.R. Breese, C. Adams, D. Patterson, L.E. Adler, L. Kruglyak, S. Leonard, and W. Byerley Linkage of a neuropsychological deficit in schizophrenia to a chromosome 15 locus Proc. Natl. Acad. Sci. USA 94 1997 587 592
23. R. Freedman, S. Leonard, J.M. Gault, J. Hopkins, C.R. Cloninger, C.A. Kaufmann, M.T. Tsuang, S.V. Farone, D. Malaspina, D.M. Svrakic, A. Sanders, and P. Gejman Linkage disequilibrium for schizophrenia at the chromosome 15q13-14 locus of the alpha7- nicotinic acetylcholine receptor subunit gene (CHRNA7) Am. J. Med. Genet. 105 2001 20 22
24. R. Freedman, A. Olincy, R.W. Buchanan, J.G. Harris, J.M. Gold, L. Johnson, D. Allensworth, A. Guzman-Bonilla, B. Clement, M.P. Ball, J. Kutnick, V. Pender, L.F. Martin, K.E. Stevens, B.D. Wagner, G.O. Zerbe, F. Soti, and W.R. Kem Initial phase 2 trial of a nicotinic agonist in schizophrenia Am. J. Psychiatry 165 2008 1040 1047
25. D.R. Fuerst, J. Gallinat, and N.N. Boutros Range of sensory gating values and test-retest reliability in normal subjects Psychophysiology 44 2007 620 626
26. J.K. Gill, M. Savolainen, G.T. Young, R. Zwart, E. Sher, and N.S. Millar Agonist activation of alpha7 nicotinic acetylcholine receptors via an allosteric transmembrane site Proc. Natl. Acad. Sci. USA 108 2011 5867 5872
27. R.J. Gurrera, D.F. Salisbury, B.F. O'Donnell, P.G. Nestor, and R.W. McCarley Auditory P3 indexes personality traits and cognitive function in healthy men and women Psychiatry Res. 133 2005 215 228
28. M. Hajós, and B.N. Rogers Targeting alpha7 nicotinic acetylcholine receptors in the treatment of schizophrenia Curr. Pharm. Des. 16 2010 538 554
29. A.S. Hedayat, and M. Yang Optimal and efficient crossover designs for comparing test treatments with a control treatment Ann. Statist. 33 2005 915 943
30. I. Helbig, H.C. Mefford, A.J. Sharp, M. Guipponi, M. Fichera, A. Franke, H. Muhle, C. de Kovel, C. Baker, S. von Spiczak, K.L. Kron, I. Steinich, A.A. Kleefuss-Lie, C. Leu, V. Gaus, B. Schmitz, K.M. Klein, P.S. Reif, F. Rosenow, Y. Weber, H. Lerche, F. Zimprich, L. Urak, K. Fuchs, M. Feucht, P. Genton, P. Thomas, F. Visscher, G.J. de Haan, R.S. Moller, H. Hjalgrim, D. Luciano, M. Wittig, M. Nothnagel, C.E. Elger, P. Nürnberg, C. Romano, A. Malafosse, B.P. Koeleman, D. Lindhout, U. Stephani, S. Schreiber, E.E. Eichler, and T. Sander 15q13.3 microdeletions increase risk of idiopathic generalized epilepsy Nat. Genet. 41 2009 160 162
31. International Schizophrenia Consortium Rare chromosomal deletions and duplications increase risk of schizophrenia Nature 455 2008 237 241
32. M. Ishikawa, and K. Hashimoto α7 nicotinic acetylcholine receptor as a potential therapeutic target for schizophrenia Curr. Pharm. Des. 17 2011 121 129
33. D.C. Javitt, K.M. Spencer, G.K. Thaker, G. Winterer, and M. Hajós Neurophysiological biomarkers for drug development in schizophrenia Nat. Rev. Drug Discov. 7 2008 68 83
34. R. Johnson Jr. A triarchic model of P300 amplitude Psychophysiology 23 1986 367 384
35. K.S. Kroker, G. Rast, and H. Rosenbrock Differential effects of subtype-specific nicotinic acetylcholine receptor agonists on early and late hippocampal LTP Eur. J. Pharmacol. 671 2011 26 32
36. S. Leonard, and R. Freedman Genetics of chromosome 15q13-q14 in schizophrenia Biol. Psychiatry 60 2006 115 122
37. S. Leonard, J. Gault, T. Moore, J. Hopkins, M. Robinson, A. Olincy, L.E. Adler, C.R. Cloninger, C.A. Kaufmann, M.T. Tsuang, S.V. Faraone, D. Malaspina, D.M. Svrakic, and R. Freedman Further investigation of a chromosome 15 locus in schizophrenia: analysis of affected sibpairs from the NIMH genetics initiative Am. J. Med. Genet. 81 1998 308 312
38. S. Leonard, C. Breese, C. Adams, K. Benhammou, J. Gault, K. Stevens, M. Lee, L. Adler, A. Olincy, R. Ross, and R. Freedman Smoking and schizophrenia: abnormal nicotinic receptor expression Eur. J. Pharmacol. 393 2000 237 242
39. S. Leonard, J. Gault, J. Hopkins, J. Logel, R. Vianzon, M. Short, C. Drebing, R. Berger, D. Venn, P. Sirota, G. Zerbe, A. Olincy, R.G. Ross, L.E. Adler, and R. Freedman Association of promoter variants in the alpha7 nicotinic acetylcholine receptor subunit gene with an inhibitory deficit found in schizophrenia Arch. Gen. Psychiatry 59 2002 1085 1096
40. S. Leonard, S. Mexal, and R. Freedman Smoking, genetics and schizophrenia: evidence for self medication J. Dual Diagn. 3 2007 43 59
41. J.G. Li, M. Lehr, L.Y. Liu-Chen, and D.S. Woodruff-Pak Nicotinic acetylcholine receptors and modulation of learning in 4- and 27-month-old rabbits Neuropsychopharmacology 33 2008 2820 2830
42. J.A. Lieberman, J.A. Javitch, and H. Moore Cholinergic agonists as novel treatments for schizophrenia: the promise of rational drug development for psychiatry Am. J. Psychiatry 165 2008 931 936
43. C. Luckhaus, U. Henning, S. Ferrea, F. Musso, A. Mobascher, and G. Winterer Nicotinic acetylcholine receptor expression on B-lymphoblasts of healthy versus schizophrenic subjects stratified for smoking: [3H]-nicotine binding is decreased in schizophrenia and correlates with negative symptoms J. Neural Transm. 119 2012 587 595
44. J. Malysz, J. Halvard Gronlien, D.J. Anderson, M. Håkerud, K. Thorin-Hagene, H. Ween, C. Wetterstrand, C.A. Briggs, R. Faghih, W.H. Bunnelle, and M. Gopalakrishnan In vitro pharmacological characterization of a novel allosteric modulator of α7 neuronal acetylcholine receptor, 4-(5-(4-chlorophenyl)-2-methyl-3-propionyl-1H-pyrrol-1-yl)benzenesulfonamide (A-867744), exhibiting unique pharmacological profile J. Pharmacol. Exp. Ther. 330 2009 257 267
45. T.A. Manolio, F.S. Collins, N.J. Cox, D.B. Goldstein, L.A. Hindorff, D.J. Hunter, M.I. McCarthy, E.M. Ramos, L.R. Cardon, A. Chakravarti, J.H. Cho, A.E. Guttmacher, A. Kong, L. Kruglyak, E. Mardis, C.N. Rotimi, M. Slatkin, D. Valle, A.S. Whittemore, M. Boehnke, A.G. Clark, E.E. Eichler, G. Gibson, J.L. Haines, T.F. Mackay, S.A. McCarroll, and P.M. Visscher Finding the missing heritability of complex diseases Nature 461 2009 747 753
46. M.J. Marks, P. Whiteaker, S.R. Grady, M.R. Picciotto, J.M. McIntosh, and A.C. Collins Characterization of [(125) I]epibatidine binding and nicotinic agonist-mediated (86) Rb(+) efflux in interpeduncular nucleus and inferior colliculus of beta2 null mutant mice J. Neurochem. 81 2002 1102 1115
47. D.T. Miller, Y. Shen, L.A. Weiss, J. Korn, I. Anselm, C. Bridgemohan, G.F. Cox, H. Dickinson, J. Gentile, D.J. Harris, V. Hegde, R. Hundley, O. Khwaja, S. Kothare, C. Luedke, R. Nasir, A. Poduri, K. Prasad, P. Raffalli, A. Reinhard, S.E. Smith, M.M. Sobeih, J.S. Soul, J. Stoler, M. Takeoka, W.H. Tan, J. Thakuria, R. Wolff, R. Yusupov, J.F. Gusella, M.J. Daly, and B.L. Wu Microdeletion/duplication at 15q13.2q13.3 among individuals with features of autism and other neuropsychiatric disorders J. Med. Genet. 46 2009 242 248
48. A. Mobascher, J. Brinkmeyer, T. Warbrick, C. Wels, M. Wagner, G. Gründer, K.N. Spreckelmeyer, T. Wienker, A. Diaz-Lacava, N. Dahmen, M. Böttcher, N. Thuerauf, M. Clepce, F. Kiefer, W. De Millas, J. Gallinat, and G. Winterer The P300 event-related potential and smoking-a population-based case-control study Int. J. Psychophysiol. 77 2010 166 175
49. S. Moriguchi, N. Shioda, F. Han, J.Z. Yeh, T. Narahashi, and K. Fukunaga Galantamine enhancement of long-term potentiation is mediated by calcium/calmodulin-dependent protein kinase II and protein kinase C activation Hippocampus 19 2009 844 854
50. F. Musso, J. Brinkmeyer, D. Ecker, M.K. London, G. Thieme, T. Warbrick, H.J. Wittsack, A. Saleh, W. Greb, P. de Boer, and G. Winterer Ketamine effects on brain function-simultaneous fMRI/EEG during a visual oddball task Neuroimage 58 2011 508 525
51. H.T. Nagamoto, L.E. Adler, M.C. Waldo, J. Griffith, and R. Freedman Gating of auditory response in schizophrenics and normal controls. Effects of recording site and stimulation interval on the P50 wave Schizophr. Res. 4 1991 31 40
52. H.T. Nagamoto, L.E. Adler, K.A. McRae, P. Huettl, E. Cawthra, G. Gerhardt, R. Hea, and J. Griffith Auditory P50 in schizophrenics on clozapine: improved gating parallels clinical improvement and changes in plasma 3-methoxy-4-hydroxyphenylglycol Neuropsychobiology 39 1999 10 17
53. A. Olincy, and K.E. Stevens Treating schizophrenia symptoms with an alpha7 nicotinic agonist, from mice to men Biochem. Pharmacol. 74 2007 1192 1201
54. A. Olincy, J.G. Harris, L.L. Johnson, V. Pender, S. Kongs, D. Allensworth, J. Ellis, G.O. Zerbe, S. Leonard, K.E. Stevens, J.O. Stevens, L. Martin, L.E. Adler, F. Soti, W.R. Kem, and R. Freedman Proof-of-concept trial of an alpha7 nicotinic agonist in schizophrenia Arch. Gen. Psychiatry 63 2006 630 638
55. R.L. Papke, W.R. Kem, F. Soti, G.Y. Lopez-Hernandez, and N.A. Horenstein Activation and desensitization of nicotinic alpha7-type acetylcholine receptors by benzylidene anabaseines and nicotine J. Pharmacol. Exp. Ther. 329 2009 791 807
56. P. Pichat, O.E. Bergis, J.P. Terranova, A. Urani, C. Duarte, V. Santucci, C. Gueudet, C. Voltz, R. Steinberg, J. Stemmelin, F. Oury-Donat, P. Avenet, G. Griebel, and B. Scatton SSR180711, a novel selective alpha7 nicotinic receptor partial agonist: (II) efficacy in experimental models predictive of activity against cognitive symptoms of schizophrenia Neuropsychopharmacology 32 2007 17 34
57. J.G. Pigeon, and D. Raghavarao Crossover designs for comparing treatments with a control Biometrika 74 1987 321 328
58. R.B. Poorthuis, N.A. Goriounova, J.J. Couey, and H.D. Mansvelder Nicotinic actions on neuronal networks for cognition: general principles and long-term consequences Biochem. Pharmacol. 78 2009 668 676
59. R. Portin, T. Kovala, P. Polo-Kantola, A. Revonsuo, K. Muller, and E. Matikainen Does P3 reflect attentional or memory performances, or cognition more generally? Scand. J. Psychol. 41 2000 31 40
60. B.B. Quednow, J. Brinkmeyer, A. Mobascher, M. Nothnagel, F. Musso, G. Gründer, N. Savary, N. Petrovsky, I. Frommann, L. Lennertz, K.N. Spreckelmeyer, T. Wienker, N. Dahmen, N. Thuerauf, M. Clepce, F. Kiefer, T. Majic, R. Mössner, W. Maier, J. Gallinat, A. Díaz-Lacava, M.R. Toliat, H. Thiele, P. Nürnberg, M. Wagner, and G. Winterer Schizophrenia risk polymorphisms in the TCF4 gene interact with smoking in the modulation of auditory sensory gating Proc. Natl. Acad. Sci. U S A 2012 [Epub ahead of print]
61. P. Russo, and A. Taly Alpha7 nicotinic acetylcholine receptors: an old actor for new different roles Curr. Drug Targets 2012 [Epub ahead of print]
62. N.J. Schork, S.S. Murray, K.A. Frazer, and E.J. Topol Common vs. rare allele hypotheses for complex diseases Curr. Opin. Genet. Dev. 19 2009 212 219
63. A.J. Sharp, H.C. Mefford, K. Li, C. Baker, C. Skinner, R.E. Stevenson, R.J. Schroer, F. Novara, M. De Gregori, R. Ciccone, A. Broomer, I. Casuga, Y. Wang, C. Xiao, C. Barbacioru, G. Gimelli, B.D. Bernardina, C. Torniero, R. Giorda, R. Regan, V. Murday, S. Mansour, M. Fichera, L. Castiglia, P. Failla, M. Ventura, Z. Jiang, G.M. Cooper, S.J. Knight, C. Romano, O. Zuffardi, C. Chen, C.E. Schwartz, and E.E. Eichler A recurrent 15q13.3 microdeletion syndrome associated with mental retardation and seizures Nat. Genet. 40 2008 322 328
64. J.K. Simosky, K.E. Stevens, L.E. Adler, and R. Freedman Clozapine improves deficient inhibitory auditory processing in DBA/2 mice, via a nicotinic cholinergic mechanism Psychopharmacology (Berl) 165 2003 386 396
65. H. Stefansson, D. Rujescu, S. Cichon, O.P. Pietiläinen, A. Ingason, S. Steinberg, R. Fossdal, E. Sigurdsson, T. Sigmundsson, J.E. Buizer-Voskamp, T. Hansen, K.D. Jakobsen, P. Muglia, C. Francks, P.M. Matthews, A. Gylfason, B.V. Halldorsson, D. Gudbjartsson, T.E. Thorgeirsson, A. Sigurdsson, A. Jonasdottir, A. Jonasdottir, A. Bjornsson, S. Mattiasdottir, T. Blondal, M. Haraldsson, B.B. Magnusdottir, I. Giegling, H.J. Möller, A. Hartmann, K.V. Shianna, D. Ge, A.C. Need, C. Crombie, G. Fraser, N. Walker, J. Lonnqvist, J. Suvisaari, A. Tuulio-Henriksson, T. Paunio, T. Toulopoulou, E. Bramon, M. Di Forti, R. Murray, M. Ruggeri, E. Vassos, S. Tosato, M. Walshe, T. Li, C. Vasilescu, T.W. Mühleisen, A.G. Wang, H. Ullum, S. Djurovic, I. Melle, J. Olesen, L.A. Kiemeney, B. Franke, C. Sabatti, N.B. Freimer, J.R. Gulcher, U. Thorsteinsdottir, A. Kong, O.A. Andreassen, R.A. Ophoff, A. Georgi, M. Rietschel, T. Werge, H. Petursson, D.B. Goldstein, M.M. Nöthen, L. Peltonen, D.A. Collier, D. St Clair, and K. Stefansson Large recurrent microdeletions associated with schizophrenia Nature 455 2008 232 236
66. K.E. Stevens, and K.D. Wear Normalizing effects of nicotine and a novel nicotinic agonist on hippocampal auditory gating in two animal models Pharmacol. Biochem. Behav. 57 1997 869 874
67. N. Thirugnanasambandam, J. Grundey, K. Adam, A. Drees, A.C. Skwirba, N. Lang, W. Paulus, and M.A. Nitsche Nicotinergic impact on focal and non-focal neuroplasticity induced by non-invasive brain stimulation in non-smoking humans Neuropsychopharmacology 36 2011 879 886
68. M.S. Thomsen, and J.D. Mikkelsen The alpha7 nicotinic acetylcholine receptor complex: one, two or multiple drug targets Curr. Drug Targets 2012 [Epub ahead of print]
69. M.S. Thomsen, H.H. Hansen, D.B. Timmerman, and J.D. Mikkelsen Cognitive improvement by activation of alpha7 nicotinic acetylcholine receptors: from animal models to human pathophysiology Curr. Pharm. Des. 16 2010 323 343
70. M.S. Thomsen, M. El-Sayed, and J.D. Mikkelsen Differential immediate and sustained memory enhancing effects of alpha7 nicotinic receptor agonists and allosteric modulators in rats PLoS One 6 2011 e27014
71. M.C. Waldo, E. Cawthwra, L.E. Adler, S. Dubester, M. Staunton, H. Nagamoto, N. Baker, A. Madison, J. Simon, and A. Scherzinger Auditory sensory gating, hippocampal volume, and catecholamine metabolism in schizophrenics and their siblings Schizophr. Res. 12 1994 93 106
72. L. Wan, H.J. Crawford, and N. Boutros P50 sensory gating: impact of high vs. low schizotypal personality and smoking status Int. J. Psychophysiol. 60 2006 1 9
73. L. Wan, H.J. Crawford, and N.N. Boutros Early and late auditory sensory gating: moderating influences from schizotypal personality, tobacco smoking status, and acute smoking Psychiatry Res. 151 2007 11 20
74. T. Warbrick, A. Mobascher, J. Brinkmeyer, F. Musso, S. Stoecker, N.J. Shah, and G. Winterer Nicotine effects on brain function during a visual oddball task: a comparison between conventional and EEG-informed fMRI analysis J. Cogn. Neurosci. 2012 [Epub ahead of print]
75. N.M. Williams, B. Franke, E. Mick, R.J. Anney, C.M. Freitag, M. Gill, A. Thapar, M.C. O'Donovan, M.J. Owen, P. Holmans, L. Kent, F. Middleton, Y. Zhang-James, L. Liu, J. Meyer, T.T. Nguyen, J. Romanos, M. Romanos, C. Seitz, T.J. Renner, S. Walitza, A. Warnke, H. Palmason, J. Buitelaar, N. Rommelse, A.A. Vasquez, Z. Hawi, K. Langley, J. Sergeant, H.C. Steinhausen, H. Roeyers, J. Biederman, I. Zaharieva, H. Hakonarson, J. Elia, A.C. Lionel, J. Crosbie, C.R. Marshall, R. Schachar, S.W. Scherer, A. Todorov, S.L. Smalley, S. Loo, S. Nelson, C. Shtir, P. Asherson, A. Reif, K.P. Lesch, and S.V. Faraone Genome-wide analysis of copy number variants in attention deficit hyperactivity disorder: the role of rare variants and duplications at 15q13.3 Am. J. Psychiatry 169 2012 195 204
76. G. Winterer Translational medicine: functional biomarkers for drug development of "cognitive enhancers" in schizophrenia M. Ritsner, Neuropsychiatric Biomarkers, Endophenotypes, and Genes: Promises, Advances and Challenges Neuropsychological Endophenotypes and Biomarkers vol. I 2009 Springer Berlin 57 86
77. G. Winterer Why do patients with schizophrenia smoke? Curr. Opin. Psychiatry 23 2010 112 119
78. G. Winterer, and R. McCarley Electrophysiology of schizophrenia D.R. Weinberger, P.J. Harrison, Schizophrenia third ed. 2011 Blackwell Publishing Oxford
79. G.T. Young, R. Zwart, A.S. Walker, E. Sher, and N.S. Millar Potentiation of alpha7 nicotinic acetylcholine receptors via an allosteric transmembrane site Proc. Natl. Acad. Sci. U S A 105 2008 14686 14691
80. D. Ziedonis, B. Hitsman, J.C. Beckham, M. Zvolensky, L.E. Adler, J. Audrain-McGovern, N. Breslau, R.A. Brown, T.P. George, J. Williams, P.S. Calhoun, and W.T. Riley Tobacco use and cessation in psychiatric disorders: national institute of mental health report Nicotine Tob. Res. 10 2008 1691 1715