Subtype-selective nicotinic acetylcholine receptor agonists can improve cognitive flexibility in an attentional set shifting task

Neuropharmacology

Volumn 105, Issue , 2016, Pages 106-113

  Wood, Christopher ^a   Kohli, Shivali ^a   Malcolm, Emma ^a   Allison, Claire ^a   Shoaib, Mohammed ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

Attention; Cognition; Ketamine; Nicotine; Rat

Indexed keywords

1 (5 CHLORO 2,4 DIMETHOXYPHENYL) 3 (5 METHYL 3 ISOXAZOLYL)UREA; 1,4 DIAZABICYCLO[3.2.2]NONANE 4 CARBOXYLIC ACID 4 BROMOPHENYL ESTER; 5 IA 85380; BUNGAROTOXIN RECEPTOR; CHOLINERGIC RECEPTOR STIMULATING AGENT; COMPOUND A; KETAMINE; NICOTINIC RECEPTOR BETA2; NICOTINIC RECEPTOR BLOCKING AGENT; UNCLASSIFIED DRUG; 1-(5-CHLORO-2,4-DIMETHOXYPHENYL)-3-(5-METHYLISOXAZOL-3-YL)UREA; CARBANILAMIDE DERIVATIVE; FUSED HETEROCYCLIC RINGS; ISOXAZOLE DERIVATIVE; NICOTINE; NICOTINIC AGENT; NICOTINIC RECEPTOR;

ANIMAL EXPERIMENT; ARTICLE; ATTENTION DEFICIT DISORDER; ATTENTIONAL SET SHIFTING TASK; COGNITION; COGNITIVE FLEXIBILITY; CONTROLLED STUDY; DRUG EFFICACY; HABITUATION; LOW DRUG DOSE; MALE; MENTAL PERFORMANCE; NONHUMAN; OLFACTORY DISCRIMINATION; PERCEPTIVE DISCRIMINATION; PRIORITY JOURNAL; RAT; TASK PERFORMANCE; AGONISTS; ANIMAL; ATTENTION; DECISION MAKING; DRUG EFFECTS; PHYSIOLOGY;

ALPHA7 NICOTINIC ACETYLCHOLINE RECEPTOR; ANIMALS; ATTENTION; BRIDGED BICYCLO COMPOUNDS, HETEROCYCLIC; CHOICE BEHAVIOR; COGNITION; DISCRIMINATION (PSYCHOLOGY); ISOXAZOLES; MALE; NICOTINE; NICOTINIC AGONISTS; PHENYLUREA COMPOUNDS; RATS; RECEPTORS, NICOTINIC;

EID: 84955144875     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2016.01.006     Document Type: Article

References (56)

1. C.G. AhnAllen, P.G. Nestor, M.E. Shenton, R.W. McCarley, and M.A. Niznikiewicz Early nicotine withdrawal and transdermal nicotine effects on neurocognitive performance in schizophrenia Schizophr. Res. 100 2008 261 269
2. M. Alkondon, E.F. Pereira, W.S. Cortes, A. Maelicke, and E.X. Albuquerque Choline is a selective agonist of alpha7 nicotinic acetylcholine receptors in the rat brain neurons Eur. J. Neurosci. 9 1997 2734 2742
3. C. Allison, and M. Shoaib Nicotine improves performance in an attentional set shifting task in rats Neuropharmacology 64 2013 314 320
4. J.T. Andreasen, J.P. Redrobe, and E.Ø. Nielsen Combined α7 nicotinic acetylcholine receptor agonism and partial serotonin transporter inhibition produce antidepressant-like effects in the mouse forced swim and tail suspension tests: a comparison of SSR180711 and PNU-282987 J. Pharmacol. Biochem. Behav. 100 3 2012 624 629
5. G.W. Arendash, G.J. Sengstock, P.R. Sanberg, and W.R. Kem Improved learning and memory in aged rats with chronic administration of the nicotinic receptor agonist GTS-21 Brain Res. 674 1995 252 259
6. J. Arnt, B. Bang-Andersen, B. Grayson, F.P. Bymaster, M.P. Cohen, N.W. DeLapp, B. Giethlen, M. Kreilgaard, D.L. McKinzie, J.C. Neill, D.L. Nelson, S.M. Nielsen, M.N. Poulsen, J.M. Schaus, and L.M. Witten Lu AE58054, a 5-HT6 antagonist, reverses cognitive impairment induced by subchronic phencyclidine in a novel object recognition test in rats Int. J. Neuropsychopharmacol. 13 2010 1021 1033
7. R.S. Barr, M.A. Culhane, L.E. Jubelt, R.S. Mufti, M.A. Dyer, A.P. Weiss, T. Deckersbach, J.F. Kelly, O. Freudenreich, D.C. Goff, and A.E. Evins The effects of transdermal nicotine on cognition in nonsmokers with schizophrenia and nonpsychiatric controls Neuropsychopharmacology 33 2008 480 490
8. J.M. Birrell, and V.J. Brown Medial frontal cortex mediates perceptual attentional set shifting in the rat J. Neurosci. 20 2000 4320 4324
9. B. Biton, O.E. Bergis, F. Galli, A. Nedelec, A.W. Lochead, S. Jegham, D. Godet, C. Lanneau, R. Santamaria, F. Chesney, J. Léonardon, P. Granger, M.W. Debono, G.A. Bohme, F. Sgard, F. Besnard, D. Graham, A. Coste, A. Oblin, O. Curet, X. Vigé, C. Voltz, L. Rouquier, J. Souilhac, V. Santucci, C. Gueudet, D. Françon, R. Steinberg, G. Griebel, F. Oury-Donat, P. George, P. Avenet, and B. Scatton SSR180711, a novel selective alpha7 nicotinic receptor partial agonist: (1) binding and functional profile Neuropsychopharmacology 32 1 2007 1 16
10. M. Bubser, T.M. Bridges, D. Dencker, R.W. Gould, M. Grannan, M.J. Noetzel, A. Lamsal, C.M. Niswender, J.S. Daniels, M.S. Poslusney, B.J. Melancon, J.C. Tarr, F.W. Byers, J. Wess, M.E. Duggan, J. Dunlop, M.W. Wood, N.J. Brandon, M.R. Wood, C.W. Lindsley, P.J. Conn, and C.K. Jones Selective activation of M4 muscarinic acetylcholine receptors reverses MK-801-induced behavioral impairments and enhances associative learning in rodents ACS Chem. Neurosci. 5 2014 920 942
11. J.J. Buccafusco, and A.V. Terry Jr. A reversible model of the cognitive impairment associated with schizophrenia in monkeys: potential therapeutic effects of two nicotinic acetylcholine receptor agonists Biochem. Pharmacol. 78 2009 852 862
12. A.E. Ceaser, T.E. Goldberg, M.F. Egan, R.P. McMahon, D.R. Weinberger, and J.M. Gold Set-shifting ability and schizophrenia: a marker of clinical illness or an intermediate phenotype? Biol. Psychiatry 64 2008 782 788
13. M.J. Chandley, M.N. Miller, C.N. Kwasigroch, T.D. Wilson, and B.E. Miller Increased antibodies for the alpha7 subunit of the nicotinic receptor in schizophrenia Schizophr. Res. 109 2009 98 101
14. S. Chapman, M. Ragg, and K. McGeechan Citation bias in reported smoking prevalence in people with schizophrenia Aust. N. Z. J. Psychiatry 43 2009 277 282
15. J. Cilia, J.E. Cluderay, M.J. Robbins, C. Reavill, E. Southam, J.N. Kew, and D.N. Jones Reversal of isolation-rearing-induced PPI deficits by an alpha7 nicotinic receptor agonist Psychopharmacol. Berl. 182 2005 214 219
16. J.W. Dalley, R.N. Cardinal, and T.W. Robbins Prefrontal executive and cognitive functions in rodents: neural and neurochemical substrates Neurosci. Biobehav Rev. 28 2004 771 784
17. V. De Luca, A.H.C. Wong, D.J. Muller, G.W.H. Wong, R.F. Tyndale, and J.L. Kennedy Evidence of association between smoking and [alpha]7 nicotinic receptor subunit gene in schizophrenia patients Neuropsychopharmacology 29 2004 1522 1526
18. Y.S. Ding, S.J. Gatley, J.S. Fowler, N.D. Volkow, D. Aggarwal, J. Logan, S.L. Dewey, F. Liang, F.I. Carroll, and M.J. Kuhar Mapping nicotinic acetylcholine receptors with PET Synapse 24 1996 403 407
19. L. Fellini, G. Kumar, S. Gibbs, T. Steckler, and J. Talpos Re-evaluating the PCP challenge as a pre-clinical model of impaired cognitive flexibility in schizophrenia Eur. Neuropsychopharmacol. 24 11 2014 1836 1849
20. S.B. Floresco, Y. Zhang, and T. Enomoto Neural circuits subserving behavioral flexibility and their relevance to schizophrenia Behav. Brain Res. 204 2009 396 409
21. 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
22. 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
23. Z. Gil, B.W. Connors, and Y. Amitai Differential regulation of neocortical synapses by neuromodulators and activity Neuron 19 1997 679 686
24. G. Gilmour, S. Dix, L. Fellini, F. Gastambide, N. Plath, T. Steckler, J. Talpos, and M. Tricklebank NMDA receptors, cognition and schizophrenia-testing the validity of the NMDA receptor hypofunction hypothesis Neuropharmacology 62 2012 1401 1412
25. 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
26. C. Gotti, and F. Clementi Neuronal nicotinic receptors: from structure to pathology Prog. Neurobiol. 74 2004 363 396
27. 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
28. J.D. Jentsch, and R.H. Roth The neuropsychopharmacology of phencyclidine: from NMDA receptor hypofunction to the dopamine hypothesis of schizophrenia Neuropsychopharmacology 20 1999 201 225
29. W.R. Kem The brain alpha7 nicotinic receptor may be an important therapeutic target for the treatment of Alzheimer's disease: studies with DMXBA (GTS-21) Behav. Brain Res. 113 2000 169 181
30. 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
31. A.C. Lahti, H.H. Holcomb, X.-M. Gao, and C.A. Tamminga NMDA-sensitive glutamate antagonism: a human model for psychosis Neuropsychopharmacology 21 1999 S158 S169
32. V.C. Leeson, T.W. Robbins, E. Matheson, S.B. Hutton, M.A. Ron, T.R. Barnes, and E.M. Joyce Discrimination learning, reversal, and set-shifting in first-episode schizophrenia: stability over six years and specific associations with medication type and disorganization syndrome Biol. Psychiatry 66 2009 586 593
33. P. Livingstone, J. Dickinson, J. Srinivasan, J.C. Kew, and S. Wonnacott Glutamate-Dopamine crosstalk in the rat prefrontal cortex is modulated by Alpha7 nicotinic receptors and potentiated by PNU-120596 J. Mol. Neurosci. 40 2010 172 176
34. J. McKirdy, J.E. Sussmann, J. Hall, S.M. Lawrie, E.C. Johnstone, and A.M. McIntosh Set shifting and reversal learning in patients with bipolar disorder or schizophrenia Psychol. Med. 39 2009 1289 1293
35. 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
36. 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 α7 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
37. 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
38. E.M. Meyer, E.T. Tay, J.A. Zoltewicz, C. Meyers, M.A. King, R.L. Papke, and et al. Neuroprotective and memory-related actions of novel alpha-7 nicotinic agents with different mixed agonist/antagonist properties J. Pharmacol. Exp. Ther. 284 1998 1026 1032
39. H. Miyata Role of smoking and nicotine in neuropsychiatric disorders: evidence for therapeutic role of nicotinic acetylcholine receptors Nihon Shinkei Seishin Yakurigaku Zasshi 28 2008 149 158
40. 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
41. 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
42. 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
43. B.W. Palmer, R.K. Heaton, J.S. Paulsen, J. Kuck, D. Braff, M.J. Harris, S. Zisook, and D.V. Jeste Is it possible to be schizophrenic yet neuropsychologically normal? Neuropsychology 11 1997 437 446
44. 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 1 2007 17 34
45. J.S. Rodefer, E.R. Murphy, M.G. Baxter, J.S. Rodefer, E.R. Murphy, and M.G. Baxter PDE10A inhibition reverses subchronic PCP-induced deficits in attentional set-shifting in rats Eur. J. Neurosci. 21 2005 1070 1076
46. J.S. Rodefer, T.N. Nguyen, J.J. Karlsson, and J. Arnt Reversal of subchronic PCP-induced deficits in attentional set shifting in rats by sertindole and a 5-HT(6) receptor antagonist: comparison among antipsychotics Neuropsychopharmacology 33 2008 2657 2666
47. S.L. Rushforth, C. Allison, S. Wonnacott, and M. Shoaib Subtype-selective nicotinic agonists enhance olfactory working memory in normal rats: a novel use of the odour span task Neurosci. Lett. 471 2010 114 118
48. S.L. Rushforth, T. Steckler, and M. Shoaib Nicotine improves working memory span capacity in rats following sub-chronic ketamine exposure Neuropsychopharmacology 36 2011 2774 2781
49. K.A. Sacco, K.L. Bannon, and T.P. George Nicotinic receptor mechanisms and cognition in normal states and neuropsychiatric disorders J. Psychopharmacol. 18 2004 457 474
50. K.A. Sacco, A. Termine, A. Seyal, M.M. Dudas, J.C. Vessicchio, S. Krishnan-Sarin, P.I. Jatlow, B.E. Wexler, and T.P. George Effects of cigarette smoking on spatial working memory and attentional deficits in schizophrenia: involvement of nicotinic receptor mechanisms Arch. Gen. Psychiatry 62 2005 649 659
51. J.W. Smith, F. Gastambide, G. Gilmour, S. Dix, J. Foss, K. Lloyd, N. Malik, and M. Tricklebank A comparison of the effects of ketamine and phencyclidine with other antagonists of the NMDA receptor in rodent assays of attention and working memory Psychopharmacol. Berl. 217 2011 255 269
52. H. Stefansson, D. Rujescu, S. Cichon, O.P. Pietilainen, 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. Moller, 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. Muhleisen, 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. Nothen, L. Peltonen, D.A. Collier, D. St Clair, and K. Stefansson Large recurrent microdeletions associated with schizophrenia Nature 455 2008 232 236
53. J.W. Tidey, D.J. Rohsenow, G.B. Kaplan, and R.M. Swift Cigarette smoking topography in smokers with schizophrenia and matched non-psychiatric controls Drug Alcohol Depend. 80 2005 259 265
54. C. Vidal Nicotinic potentiation of glutamatergic synapses in the prefrontal cortex: new insight into the analysis of the role of nicotinic receptors in cognitive functions Drug Dev. Res. 31 1994 120 126
55. 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
56. J.W. Young, J.M. Meves, I.S. Tarantino, S. Caldwell, and M.A. Geyer Delayed procedural learning in alpha7-nicotinic acetylcholine receptor knockout mice Genes Brain Behav. 10 2011 720 733