Positive allosteric modulators of alpha 7 nicotinic acetylcholine receptors reverse ketamine-induced schizophrenia-like deficits in rats

Neuropharmacology

Volumn 101, Issue , 2016, Pages 389-400

  Nikiforuk, Agnieszka ^a   Kos, Tomasz ^a   Hołuj, Małgorzata ^a   Potasiewicz, Agnieszka ^a   Popik, Piotr ^a  

^a INSTITUTE OF PHARMACOLOGY   (Poland)

Author keywords

Alpha 7 nicotinic acetylcholine receptors; Animal models; Cognition; Ketamine; Positive allosteric modulators; Schizophrenia

Indexed keywords

1 (5 CHLORO 2,4 DIMETHOXYPHENYL) 3 (5 METHYL 3 ISOXAZOLYL)UREA; BUNGAROTOXIN RECEPTOR; GALANTAMINE; KETAMINE; N (4 CHLOROPHENYL) [[(4 CHLOROPHENYL)AMINO]METHYLENE] 3 METHYL 5 ISOXAZOLEACETAMIDE; NICOTINIC AGENT; OCTAHYDRO 2 METHYL 5 (6 PHENYL 3 PYRIDAZINYL)PYRROLO [3,4 C]PYRROLE; UNCLASSIFIED DRUG; AMINO ACID RECEPTOR BLOCKING AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIPSYCHOTIC ACTIVITY; ARTICLE; ATTENTION TEST; ATTENTIONAL SET SHIFTING TASK; AVOIDANCE BEHAVIOR; COGNITIVE DEFECT; CONTROLLED STUDY; DRUG ACTIVITY; DRUG EFFICACY; MALE; NONHUMAN; NOVEL OBJECT RECOGNITION TEST; PRIORITY JOURNAL; PSYCHOSOCIAL WITHDRAWAL; RAT; RAT MODEL; SCHIZOPHRENIA; SOCIAL INTERACTION TEST; ANALYSIS OF VARIANCE; ANIMAL; ATTENTION; BINDING SITE; CHEMICALLY INDUCED; DISEASE MODEL; DOSE RESPONSE; DRUG EFFECTS; DRUG INTERACTION; HUMAN RELATION; METABOLISM; RECOGNITION; SPRAGUE DAWLEY RAT;

ALLOSTERIC SITE; ALPHA7 NICOTINIC ACETYLCHOLINE RECEPTOR; ANALYSIS OF VARIANCE; ANIMALS; ATTENTION; AVOIDANCE LEARNING; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; EXCITATORY AMINO ACID ANTAGONISTS; INTERPERSONAL RELATIONS; KETAMINE; MALE; NICOTINIC AGONISTS; RATS; RATS, SPRAGUE-DAWLEY; RECOGNITION (PSYCHOLOGY); SCHIZOPHRENIA;

EID: 84944811073     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2015.07.034     Document Type: Article

References (72)

1. K.S. Alexander, A. Pocivavsek, H.Q. Wu, M.L. Pershing, R. Schwarcz, and J.P. Bruno Early developmental elevations of brain kynurenic acid impair cognitive flexibility in adults: reversal with galantamine Neuroscience 238 2013 19 28
2. K.S. Alexander, H.Q. Wu, R. Schwarcz, and J.P. Bruno Acute elevations of brain kynurenic acid impair cognitive flexibility: normalization by the alpha7 positive modulator galantamine Psychopharmacol. Berl. 220 2012 627 637
3. C. Allison, and M. Shoaib Nicotine improves performance in an attentional set shifting task in rats Neuropharmacology 64 2013 314 320
4. M.B. Andersen, T. Werge, and A. Fink-Jensen The acetylcholinesterase inhibitor galantamine inhibits d-amphetamine-induced psychotic-like behavior in Cebus monkeys J. Pharmacol. Exp. Ther. 321 2007 1179 1182
5. M. Bencherif, M.K. Stachowiak, A.J. Kucinski, and P.M. Lippiello Alpha7 nicotinic cholinergic neuromodulation may reconcile multiple neurotransmitter hypotheses of schizophrenia Med. Hypotheses 78 2012 594 600
6. J.M. Birrell, and V.J. Brown Medial frontal cortex mediates perceptual attentional set shifting in the rat J. Neurosci. 20 2000 4320 4324
7. J.M. Brooks, M.L. Pershing, M.S. Thomsen, J.D. Mikkelsen, M. Sarter, and J.P. Bruno Transient inactivation of the neonatal ventral hippocampus impairs attentional set-shifting behavior: reversal with an alpha7 nicotinic agonist Neuropsychopharmacology 37 2012 2476 2486
8. J.J. Buccafusco, J.W. Beach, and A.V. Terry Jr. Desensitization of nicotinic acetylcholine receptors as a strategy for drug development J. Pharmacol. Exp. Ther. 328 2009 364 370
9. R.W. Buchanan, and R. Schwarcz alpha7 Nicotinic receptor agonists as cognitive treatments: is less (or less often) more? Biol. Psychiatry 69 2011 5 6
10. P.M. Callahan, E.J. Hutchings, N.J. Kille, J.M. Chapman, and A.V. Terry Jr. Positive allosteric modulator of alpha7 nicotinic-acetylcholine receptors, PNU-120596 augments the effects of donepezil on learning and memory in aged rodents and non-human primates Neuropharmacology 67 2013 201 212
11. N. de Bruin, and B. Pouzet Beneficial effects of galantamine on performance in the object recognition task in Swiss mice: deficits induced by scopolamine and by prolonging the retention interval Pharmacol. Biochem. Behav. 85 2006 253 260
12. A. Egerton, L. Reid, C.E. McKerchar, B.J. Morris, and J.A. Pratt Impairment in perceptual attentional set-shifting following PCP administration: a rodent model of set-shifting deficits in schizophrenia Psychopharmacol. Berl. 179 2005 77 84
13. A. Ennaceur, and J. Delacour A new one-trial test for neurobiological studies of memory in rats. 1: behavioral data Behav. Brain Res. 31 1988 47 59
14. J. Eskildsen, J.P. Redrobe, A.G. Sams, K. Dekermendjian, M. Laursen, J.B. Boll, R.L. Papke, C. Bundgaard, K. Frederiksen, and J.F. Bastlund Discovery and optimization of Lu AF58801, a novel, selective and brain penetrant positive allosteric modulator of alpha-7 nicotinic acetylcholine receptors: Attenuation of subchronic phencyclidine (PCP)-induced cognitive deficits in rats following oral administration Bioorg Med. Chem. Lett. 24 2014 288 293
15. 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 neurophysiological deficit in schizophrenia to a chromosome 15 locus Proc. Natl. Acad. Sci. U. S. A. 94 1997 587 592
16. 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
17. F. Gastambide, S.N. Mitchell, T.W. Robbins, M.D. Tricklebank, and G. Gilmour Temporally distinct cognitive effects following acute administration of ketamine and phencyclidine in the rat Eur. Neuropsychopharmacol. 23 2013 1414 1422
18. H. Geerts, and G.T. Grossberg Pharmacology of acetylcholinesterase inhibitors and N-methyl-D-aspartate receptors for combination therapy in the treatment of Alzheimer's disease J. Clin. Pharmacol. 46 2006 8S 16S
19. P. Goetghebeur, and R. Dias Comparison of haloperidol, risperidone, sertindole, and modafinil to reverse an attentional set-shifting impairment following subchronic PCP administration in the rat-a back translational study Psychopharmacol. Berl. 202 2009 287 293
20. Z.Z. Guan, X. Zhang, K. Blennow, and A. Nordberg Decreased protein level of nicotinic receptor alpha7 subunit in the frontal cortex from schizophrenic brain Neuroreport 10 1999 1779 1782
21. A. Gururajan, D.A. Taylor, and D.T. Malone Current pharmacological models of social withdrawal in rats: relevance to schizophrenia Behav. Pharmacol. 21 2010 690 709
22. T.A. Hauser, A. Kucinski, K.G. Jordan, G.J. Gatto, S.R. Wersinger, R.A. Hesse, E.K. Stachowiak, M.K. Stachowiak, R.L. Papke, P.M. Lippiello, and M. Bencherif TC-5619: an alpha7 neuronal nicotinic receptor-selective agonist that demonstrates efficacy in animal models of the positive and negative symptoms and cognitive dysfunction of schizophrenia Biochem. Pharmacol. 78 2009 803 812
23. M. Holuj, P. Popik, and A. Nikiforuk Improvement of ketamine-induced social withdrawal in rats: the role of 5-HT7 receptors Behav. Pharmacol. 2015 10.1097/FBP.0000000000000132
24. R.S. Hurst, M. Hajos, M. Raggenbass, T.M. Wall, N.R. Higdon, J.A. Lawson, K.L. Rutherford-Root, M.B. Berkenpas, W.E. Hoffmann, D.W. Piotrowski, V.E. Groppi, G. Allaman, R. Ogier, S. Bertrand, D. Bertrand, and S.P. Arneric A novel positive allosteric modulator of the alpha7 neuronal nicotinic acetylcholine receptor: in vitro and in vivo characterization J. Neurosci. 25 2005 4396 4405
25. C.K. Jones, N. Byun, and M. Bubser Muscarinic and nicotinic acetylcholine receptor agonists and allosteric modulators for the treatment of schizophrenia Neuropsychopharmacology 37 2012 16 42
26. K.M. Jones, I.M. McDonald, C. Bourin, R.E. Olson, L.J. Bristow, and A. Easton Effect of alpha7 nicotinic acetylcholine receptor agonists on attentional set-shifting impairment in rats Psychopharmacol. Berl. 231 2014 673 683
27. B. Kocsis, R.E. Brown, R.W. McCarley, and M. Hajos Impact of ketamine on neuronal network dynamics: translational modeling of schizophrenia-relevant deficits CNS Neurosci. Ther. 19 2013 437 447
28. M.M. Koola, R.W. Buchanan, A. Pillai, K.J. Aitchison, D.R. Weinberger, S.T. Aaronson, and F.B. Dickerson Potential role of the combination of galantamine and memantine to improve cognition in schizophrenia Schizophr. Res. 157 2014 84 89
29. J.H. Krystal, L.P. Karper, J.P. Seibyl, G.K. Freeman, R. Delaney, J.D. Bremner, G.R. Heninger, M.B. Bowers Jr., and D.S. Charney Subanesthetic effects of the noncompetitive NMDA antagonist, ketamine, in humans. Psychotomimetic, perceptual, cognitive, and neuroendocrine responses Arch. Gen. Psychiatry 51 1994 199 214
30. A. Kucinski, C. Syposs, S. Wersinger, M. Bencherif, M.K. Stachowiak, and E.K. Stachowiak alpha7 neuronal nicotinic receptor agonist (TC-7020) reverses increased striatal dopamine release during acoustic PPI testing in a transgenic mouse model of schizophrenia Schizophr. Res. 136 2012 82 87
31. S. Kunitachi, Y. Fujita, T. Ishima, M. Kohno, M. Horio, Y. Tanibuchi, Y. Shirayama, M. Iyo, and K. Hashimoto Phencyclidine-induced cognitive deficits in mice are ameliorated by subsequent subchronic administration of donepezil: role of sigma-1 receptors Brain Res. 1279 2009 189 196
32. J.A. Lieberman, G. Dunbar, A.C. Segreti, R.R. Girgis, F. Seoane, J.S. Beaver, N. Duan, and D.A. Hosford A randomized exploratory trial of an alpha-7 nicotinic receptor agonist (TC-5619) for cognitive enhancement in schizophrenia Neuropsychopharmacology 38 2013 968 975
33. J.E. Lisman, J.T. Coyle, R.W. Green, D.C. Javitt, F.M. Benes, S. Heckers, and A.A. Grace Circuit-based framework for understanding neurotransmitter and risk gene interactions in schizophrenia Trends Neurosci. 31 2008 234 242
34. P.D. Livingstone, J. Srinivasan, J.N. Kew, L.A. Dawson, C. Gotti, M. Moretti, M. Shoaib, and S. Wonnacott alpha7 and non-alpha7 nicotinic acetylcholine receptors modulate dopamine release in vitro and in vivo in the rat prefrontal cortex Eur. J. Neurosci. 29 2009 539 550
35. C. Lopes, E.F. Pereira, H.Q. Wu, P. Purushottamachar, V. Njar, R. Schwarcz, and E.X. Albuquerque Competitive antagonism between the nicotinic allosteric potentiating ligand galantamine and kynurenic acid at alpha7∗nicotinic receptors J. Pharmacol. Exp. Ther. 322 2007 48 58
36. A. Maelicke, M. Samochocki, R. Jostock, A. Fehrenbacher, J. Ludwig, E.X. Albuquerque, and M. Zerlin Allosteric sensitization of nicotinic receptors by galantamine, a new treatment strategy for Alzheimer's disease Biol. Psychiatry 49 2001 279 288
37. K.L. Marquis, T.A. Comery, F. Jow, R.L. Navarra, S.M. Grauer, C. Pulicicchio, C. Kelley, J.A. Brennan, R. Roncarati, C. Scali, S. Haydar, C. Ghiron, G.C. Terstappen, and J. Dunlop Preclinical assessment of an adjunctive treatment approach for cognitive impairment associated with schizophrenia using the alpha7 nicotinic acetylcholine receptor agonist WYE-103914/SEN34625 Psychopharmacol. Berl. 218 2011 635 647
38. S.L. McLean, B. Grayson, N.F. Idris, A.S. Lesage, D.J. Pemberton, C. Mackie, and J.C. Neill Activation of alpha7 nicotinic receptors improves phencyclidine-induced deficits in cognitive tasks in rats: implications for therapy of cognitive dysfunction in schizophrenia Eur. Neuropsychopharmacol. 21 2011 333 343
39. S.L. McLean, N.F. Idris, B. Grayson, D.F. Gendle, C. Mackie, A.S. Lesage, D.J. Pemberton, and J.C. Neill PNU-120596, a positive allosteric modulator of alpha7 nicotinic acetylcholine receptors, reverses a sub-chronic phencyclidine-induced cognitive deficit in the attentional set-shifting task in female rats J. Psychopharmacol. 26 2012 1265 1270
40. S. Mexal, R. Berger, J. Logel, R.G. Ross, R. Freedman, and S. Leonard Differential regulation of alpha7 nicotinic receptor gene (CHRNA7) expression in schizophrenic smokers J. Mol. Neurosci. 40 2010 185 195
41. R. Moaddel, G. Abdrakhmanova, J. Kozak, K. Jozwiak, L. Toll, L. Jimenez, A. Rosenberg, T. Tran, Y. Xiao, C.A. Zarate, and I.W. Wainer Sub-anesthetic concentrations of (R,S)-ketamine metabolites inhibit acetylcholine-evoked currents in alpha7 nicotinic acetylcholine receptors Eur. J. Pharmacol. 698 2013 228 234
42. J.B. Murray Phencyclidine (PCP): a dangerous drug, but useful in schizophrenia research J. Psychol. 136 2002 319 327
43. J.C. Neill, S. Barnes, S. Cook, B. Grayson, N.F. Idris, S.L. McLean, S. Snigdha, L. Rajagopal, and M.K. Harte Animal models of cognitive dysfunction and negative symptoms of schizophrenia: focus on NMDA receptor antagonism Pharmacol. Ther. 128 2010 419 432
44. H.J. Ng, E.R. Whittemore, M.B. Tran, D.J. Hogenkamp, R.S. Broide, T.B. Johnstone, L. Zheng, K.E. Stevens, and K.W. Gee Nootropic alpha7 nicotinic receptor allosteric modulator derived from GABAA receptor modulators Proc. Natl. Acad. Sci. U. S. A. 104 2007 8059 8064
45. A. Nikiforuk, K. Golembiowska, and P. Popik Mazindol attenuates ketamine-induced cognitive deficit in the attentional set shifting task in rats Eur. Neuropsychopharmacol. 20 2010 37 48
46. A. Nikiforuk, T. Kos, K. Fijal, M. Holuj, D. Rafa, and P. Popik Effects of the selective 5-HT7 receptor antagonist SB-269970 and amisulpride on ketamine-induced schizophrenia-like deficits in rats PLoS One 8 2013 e66695
47. A. Nikiforuk, T. Kos, A. Potasiewicz, and P. Popik Positive allosteric modulation of alpha 7 nicotinic acetylcholine receptors enhances recognition memory and cognitive flexibility in rats Eur. Neuropsychopharmacol. 2015 10.1016/j.euroneuro.2015.04.018
48. A. Nikiforuk, and P. Popik Effects of quetiapine and sertindole on subchronic ketamine-induced deficits in attentional set-shifting in rats Psychopharmacol. Berl. 220 2012 65 74
49. Y. Noda, A. Mouri, Y. Ando, Y. Waki, S.N. Yamada, A. Yoshimi, K. Yamada, N. Ozaki, D. Wang, and T. Nabeshima Galantamine ameliorates the impairment of recognition memory in mice repeatedly treated with methamphetamine: involvement of allosteric potentiation of nicotinic acetylcholine receptors and dopaminergic-ERK1/2 systems Int. J. Neuropsychopharmacol. 13 2010 1343 1354
50. A.A. Pandya, and J.L. Yakel Activation of the alpha7 nicotinic ACh receptor induces anxiogenic effects in rats which is blocked by a 5-HT(1)a receptor antagonist Neuropharmacology 70 2013 35 42
51. A.A. Pandya, and J.L. Yakel Effects of neuronal nicotinic acetylcholine receptor allosteric modulators in animal behavior studies Biochem. Pharmacol. 86 2013 1054 1062
52. C.S. Pedersen, D.B. Sorensen, A.I. Parachikova, and N. Plath PCP-induced deficits in murine nest building activity: employment of an ethological rodent behavior to mimic negative-like symptoms of schizophrenia Behav. Brain Res. 273 2014 63 72
53. F. Sams-Dodd Automation of the social interaction test by a video-tracking system: behavioural effects of repeated phencyclidine treatment J. Neurosci. Methods 59 1995 157 167
54. B. Schilstrom, V.B. Ivanov, C. Wiker, and T.H. Svensson Galantamine enhances dopaminergic neurotransmission in vivo via allosteric potentiation of nicotinic acetylcholine receptors Neuropsychopharmacology 32 2007 43 53
55. C. Song, T.A. Murray, R. Kimura, M. Wakui, K. Ellsworth, S.P. Javedan, S. Marxer-Miller, R.J. Lukas, and J. Wu Role of alpha7-nicotinic acetylcholine receptors in tetanic stimulation-induced gamma oscillations in rat hippocampal slices Neuropharmacology 48 2005 869 880
56. S. Sydserff, E.J. Sutton, D. Song, M.C. Quirk, C. Maciag, C. Li, G. Jonak, D. Gurley, J.C. Gordon, E.P. Christian, J.J. Doherty, T. Hudzik, E. Johnson, L. Mrzljak, T. Piser, G.N. Smagin, Y. Wang, D. Widzowski, and J.S. Smith Selective alpha7 nicotinic receptor activation by AZD0328 enhances cortical dopamine release and improves learning and attentional processes Biochem. Pharmacol. 78 2009 880 888
57. M.S. Thomsen, D.Z. Christensen, H.H. Hansen, J.P. Redrobe, and J.D. Mikkelsen alpha(7) Nicotinic acetylcholine receptor activation prevents behavioral and molecular changes induced by repeated phencyclidine treatment Neuropharmacology 56 2009 1001 1009
58. 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
59. K.R. Tietje, D.J. Anderson, R.S. Bitner, E.A. Blomme, P.J. Brackemeyer, C.A. Briggs, K.E. Browman, D. Bury, P. Curzon, K.U. Drescher, J.M. Frost, R.M. Fryer, G.B. Fox, J.H. Gronlien, M. Hakerud, E.J. Gubbins, S. Halm, R. Harris, R.J. Helfrich, K.L. Kohlhaas, D. Law, J. Malysz, K.C. Marsh, R.L. Martin, M.D. Meyer, A.L. Molesky, A.L. Nikkel, S. Otte, L. Pan, P.S. Puttfarcken, R.J. Radek, H.M. Robb, E. Spies, K. Thorin-Hagene, J.F. Waring, H. Ween, H. Xu, M. Gopalakrishnan, and W.H. Bunnelle Preclinical characterization of A-582941: a novel alpha7 neuronal nicotinic receptor agonist with broad spectrum cognition-enhancing properties CNS Neurosci. Ther. 14 2008 65 82
60. O.A. Timofeeva, and E.D. Levin Glutamate and nicotinic receptor interactions in working memory: importance for the cognitive impairment of schizophrenia Neuroscience 195 2011 21 36
61. D. Umbricht, R.S. Keefe, S. Murray, D.A. Lowe, R. Porter, G. Garibaldi, and L. Santarelli A randomized, Placebo-controlled study investigating the nicotinic alpha7 agonist, RG3487, for cognitive deficits in schizophrenia Neuropsychopharmacology 39 2014 1568 1577
62. M.L. Wadenberg Galantamine, in similarity to antipsychotic drugs, produces selective suppression of conditioned avoidance response in rats Soc. Neurosci. 198 2006 7
63. M.L. Wadenberg Conditioned avoidance response in the development of new antipsychotics Curr. Pharm. Des. 16 2010 358 370
64. M.L. Wadenberg, A.K. Fjallstrom, M. Federley, P. Persson, and P. Stenqvist Effects of adjunct galantamine to risperidone, or haloperidol, in animal models of antipsychotic activity and extrapyramidal side-effect liability: involvement of the cholinergic muscarinic receptor Int. J. Neuropsychopharmacol. 14 2011 644 654
65. M.L. Wadenberg, and P.B. Hicks The conditioned avoidance response test re-evaluated: is it a sensitive test for the detection of potentially atypical antipsychotics? Neurosci. Biobehav Rev. 23 1999 851 862
66. T.L. Wallace, P.M. Callahan, A. Tehim, D. Bertrand, G. Tombaugh, S. Wang, W. Xie, W.B. Rowe, V. Ong, E. Graham, A.V. Terry Jr., J.S. Rodefer, B. Herbert, M. Murray, R. Porter, L. Santarelli, and D.A. Lowe RG3487, a novel nicotinic alpha7 receptor partial agonist, improves cognition and sensorimotor gating in rodents J. Pharmacol. Exp. Ther. 336 2011 242 253
67. T.L. Wallace, and R.H. Porter Targeting the nicotinic alpha7 acetylcholine receptor to enhance cognition in disease Biochem. Pharmacol. 82 2011 891 903
68. D. Wang, Y. Noda, Y. Zhou, A. Mouri, H. Mizoguchi, A. Nitta, W. Chen, and T. Nabeshima The allosteric potentiation of nicotinic acetylcholine receptors by galantamine ameliorates the cognitive dysfunction in beta amyloid25-35 i.c.v.-injected mice: involvement of dopaminergic systems Neuropsychopharmacology 32 2007 1261 1271
69. D. Wang, Y. Noda, Y. Zhou, A. Nitta, H. Furukawa, and T. Nabeshima Synergistic effect of combined treatment with risperidone and galantamine on phencyclidine-induced impairment of latent visuospatial learning and memory: role of nAChR activation-dependent increase of dopamine D1 receptor-mediated neurotransmission Neuropharmacology 53 2007 379 389
70. C. Wiker, B. Schilstrom, C. Sandback, M.L. Wadenberg, and T.H. Svensson Adjunctive galantamine, but not donepezil, enhances the antipsychotic-like effect of raclopride in rats Int. J. Neuropsychopharmacol. 11 2008 845 850
71. D.K. Williams, J. Wang, and R.L. Papke Positive allosteric modulators as an approach to nicotinic acetylcholine receptor-targeted therapeutics: advantages and limitations Biochem. Pharmacol. 82 2011 915 930
72. J.W. Young, and M.A. Geyer Evaluating the role of the alpha-7 nicotinic acetylcholine receptor in the pathophysiology and treatment of schizophrenia Biochem. Pharmacol. 86 2013 1122 1132