Nicotinic agonist-induced improvement of vigilance in mice in the 5-choice continuous performance test

Behavioural Brain Research

Volumn 240, Issue 1, 2013, Pages 119-133

  Young, Jared W ^a,b   Meves, Jessica M ^a   Geyer, Mark A ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

Author keywords

Attention; Continuous performance test; Impulsivity; Nicotine; Nicotinic acetylcholine receptors; Scopolamine

Indexed keywords

3 METHYL 5 (1 METHYL 2 PYRROLIDINYL)ISOXAZOLE; 4 CHLORO N (3 QUINUCLIDINYL)BENZAMIDE; NICOTINE;

ALERTNESS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASSOCIATION; ATTENTION DEFICIT DISORDER; ATTENUATION; DOSE RESPONSE; DRUG DOSE COMPARISON; DRUG EFFECT; DRUG MECHANISM; LATENT PERIOD; MALE; MOUSE; NONHUMAN; PREDICTION; PRIORITY JOURNAL; STIMULUS RESPONSE; TASK PERFORMANCE; TREATMENT DURATION;

ANIMALS; ATTENTION; BEHAVIOR, ANIMAL; BENZAMIDES; BICYCLO COMPOUNDS; CHOICE BEHAVIOR; CHOLINERGIC ANTAGONISTS; ISOXAZOLES; MALE; MICE; MICE, INBRED C57BL; NICOTINE; NICOTINIC AGONISTS; PSYCHOMOTOR PERFORMANCE; PYRROLIDINES; RECEPTORS, NICOTINIC; SCOPOLAMINE HYDROBROMIDE;

EID: 84871377513     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2012.11.028     Document Type: Article

References (79)

1. Raedler T.J., Bymaster F.P., Tandon R., Copolov D., Dean B. Towards a muscarinic hypothesis of schizophrenia. Molecular Psychiatry 2007, 12:232-246.
2. Scarr E., Dean B. Role of the cholinergic system in the pathology and treatment of schizophrenia. Expert Review of Neurotherapeutics 2009, 9:73-86.
3. Segarra R., Zabala A., Eguiluz J.I., Ojeda N., Elizagarate E., Sanchez P., et al. Cognitive performance and smoking in first-episode psychosis: the self-medication hypothesis. European Archives of Psychiatry and Clinical Neuroscience 2010, 261(4):241-250.
4. Winterer G. Why do patients with schizophrenia smoke. Current Opinion in Psychiatry 2010, 23:112-119.
5. Kumari V., Postma P. Nicotine use in schizophrenia: the self medication hypotheses. Neuroscience and Biobehavioral Reviews 2005, 29:1021-1034.
6. Freedman R., Coon H., Myles-Worsley M., Orr-Urtreger A., Olincy A., Davis A., et al. Linkage of a neurophysiological deficit in schizophrenia to a chromosome 15 locus. Proceedings of the National Academy of Sciences of the United States of America 1997, 94:587-592.
7. Martin-Ruiz C.M., Haroutunian V.H., Long P., Young A.H., Davis K.L., Perry E.K., et al. Dementia rating and nicotinic receptor expression in the prefrontal cortex in schizophrenia. Biological Psychiatry 2003, 54:1222-1233.
8. Zavitsanou K., Katsifis A., Mattner F., Huang X.F. Investigation of m1/m4 muscarinic receptors in the anterior cingulate cortex in schizophrenia, bipolar disorder, and major depression disorder. Neuropsychopharmacology 2004, 29:619-625.
9. Deng C., Huang X.F. Decreased density of muscarinic receptors in the superior temporal gyrusin schizophrenia. Journal of Neuroscience Research 2005, 81:883-890.
10. Raedler T.J., Knable M.B., Jones D.W., Urbina R.A., Gorey J.G., Lee K.S., et al. In vivo determination of muscarinic acetylcholine receptor availability in schizophrenia. American Journal of Psychiatry 2003, 160:118-127.
11. Scarr E., Cowie T.F., Kanellakis S., Sundram S., Pantelis C., Dean B. Decreased cortical muscarinic receptors define a subgroup of subjects with schizophrenia. Molecular Psychiatry 2009, 14:1017-1023.
12. Friedman J.I. Cholinergic targets for cognitive enhancement in schizophrenia: focus on cholinesterase inhibitors and muscarinic agonists. Psychopharmacology (Berlin) 2004, 174:45-53.
13. Martin L.F., Kem W.R., Freedman R. Alpha-7 nicotinic receptor agonists: potential new candidates for the treatment of schizophrenia. Psychopharmacology (Berlin) 2004, 174:54-64.
14. Levin E.D., Conners C.K., Silva D., Hinton S.C., Meck W.H., March J., et al. Transdermal nicotine effects on attention. Psychopharmacology (Berlin) 1998, 140:135-141.
15. Rezvani A.H., Levin E.D. Cognitive effects of nicotine. Biological Psychiatry 2001, 49:258-267.
16. Heishman S.J., Kleykamp B.A., Singleton E.G. Meta-analysis of the acute effects of nicotine and smoking on human performance. Psychopharmacology (Berlin) 2010, 210:453-469.
17. Smith R.C., Warner-Cohen J., Matute M., Butler E., Kelly E., Vaidhyanathaswamy S., et al. Effects of nicotine nasal spray on cognitive function in schizophrenia. Neuropsychopharmacology 2006, 31:637-643.
18. Newhouse P., Singh A., Potter A. Nicotine and nicotinic receptor involvement in neuropsychiatric disorders. Current Topics in Medicinal Chemistry 2004, 4:267-282.
19. White H.K., Levin E.D. Four-week nicotine skin patch treatment effects on cognitive performance in Alzheimer's disease. Psychopharmacology (Berlin) 1999, 143:158-165.
20. Conners C.K., Levin E.D., Sparrow E., Hinton S.C., Erhardt D., Meck W.H., et al. Nicotine and attention in adult attention deficit hyperactivity disorder (ADHD). Psychopharmacology Bulletin 1996, 32:67-73.
21. Garvey D.S., Wasicak J.T., Decker M.W., Brioni J.D., Buckley M.J., Sullivan J.P., et al. Novel isoxazoles which interact with brain cholinergic channel receptors have intrinsic cognitive enhancing and anxiolytic activities. Journal of Medicinal Chemistry 1994, 37:1055-1059.
22. Decker M.W., Curzon P., Brioni J.D., Arneric S.P. Effects of ABT-418, a novel cholinergic channel ligand, on place learning in septal-lesioned rats. European Journal of Pharmacology 1994, 261:217-222.
23. Hurst R.S., Hajos M., Raggenbass M., Wall T.M., Higdon N.R., Lawson J.A., et al. A novel positive allosteric modulator of the alpha7 neuronal nicotinic acetylcholine receptor: in vitro and in vivo characterization. Journal of Neuroscience 2005, 25:4396-4405.
24. Hajos M., Hurst R.S., Hoffmann W.E., Krause M., Wall T.M., Higdon N.R., et al. The selective alpha7 nicotinic acetylcholine receptor agonist PNU-282987 [N-[(3R)-1-Azabicyclo[2.2.2]oct-3-yl]-4-chlorobenzamide hydrochloride] enhances GABAergic synaptic activity in brain slices and restores auditory gating deficits in anesthetized rats. Journal of Pharmacology and Experimental Therapeutics 2005, 312:1213-1222.
25. Redrobe J.P., Nielsen E.O., Christensen J.K., Peters D., Timmermann D.B., Olsen G.M. Alpha7 nicotinic acetylcholine receptor activation ameliorates scopolamine-induced behavioural changes in a modified continuous Y-maze task in mice. European Journal of Pharmacology 2009, 602:58-65.
26. Young J.W., Powell S.B., Risbrough V., Marston H.M., Geyer M.A. Using the MATRICS to guide development of a preclinical cognitive test battery for research in schizophrenia. Pharmacology & Therapeutics 2009, 122:150-202.
27. Riedel G., Kang S.H., Choi D.Y., Platt B. Scopolamine-induced deficits in social memory in mice: reversal by donepezil. Behavioural Brain Research 2009, 204:217-225.
28. de Bruin N.M., Fransen F., Duytschaever H., Grantham C., Megens A.A. Attentional performance of (C57BL/6Jx129Sv)F2 mice in the five-choice serial reaction time task. Physiology and Behavior 2006, 89:692-703.
29. Humby T., Laird F.M., Davies W., Wilkinson L.S. Visuospatial attentional functioning in mice: interactions between cholinergic manipulations and genotype. European Journal of Neuroscience 1999, 11:2813-2823.
30. Koller G., Satzger W., Adam M., Wagner M., Kathmann N., Soyka M., et al. Effects of scopolamine on matching to sample paradigm and related tests in human subjects. Neuropsychobiology 2003, 48:87-94.
31. Pattij T., Janssen M.C., Loos M., Smit A.B., Schoffelmeer A.N., van Gaalen M.M. Strain specificity and cholinergic modulation of visuospatial attention in three inbred mouse strains. Genes, Brain, and Behavior 2007, 6:579-587.
32. Young J.W., Finlayson K., Spratt C., Marston H.M., Crawford N., Kelly J.S., et al. Nicotine improves sustained attention in mice: evidence for involvement of the alpha7 nicotinic acetylcholine receptor. Neuropsychopharmacology 2004, 29:891-900.
33. Carli M., Robbins T.W., Evenden J.L., Everitt B.J. Effects of lesions to ascending noradrenergic neurones on performance of a 5-choice serial reaction task in rats; implications for theories of dorsal noradrenergic bundle function based on selective attention and arousal. Behavioural Brain Research 1983, 9:361-380.
34. Robbins T.W. The 5-choice serial reaction time task: behavioural pharmacology and functional neurochemistry. Psychopharmacology (Berlin) 2002, 163:362-380.
35. Riccio C.A., Reynolds C.R., Lowe P., Moore J.J. The continuous performance test: a window on the neural substrates for attention. Archives of Clinical Neuropsychology 2002, 17:235-272.
36. Eyler L.T., Dawes S.E., Asgaard G.L., Young J.W. Abnormalities of brain responses during vigilance and inhibition in bipolar disorder. Bipolar Disorders 2011, 13:42.
37. Fallgatter A.J. Electrophysiology of the prefrontal cortex in healthy controls and schizophrenic patients: a review. Journal of Neural Transmission 2001, 108:679-694.
38. Kleinlogel H., Strik W., Begre S. Increased NoGo-anteriorisation in first-episode schizophrenia patients during continuous performance test. Clinical Neurophysiology 2007, 118:2683-2691.
39. Young J.W., Light G.A., Marston H.M., Sharp R., Geyer M.A. The 5-choice continuous performance test: evidence for a translational test of vigilance for mice. PLoS ONE 2009, 4:e4227.
40. Lustig C., Kozak R., Sarter M., Young J.W., Robbins T.W. CNTRICS final animal model task selection: control of attention. Neuroscience and Biobehavioral Reviews 2012, in press.
41. Barnes S.A., Young J.W., Neill J.C. D(1) receptor activation improves vigilance in rats as measured by the 5-choice continuous performance test. Psychopharmacology (Berlin) 2012, 220(1):129-141.
42. Barnes S.A., Young J.W., Neill J.C. Rats tested after a washout period from sub-chronic PCP administration exhibited impaired performance in the 5-Choice Continuous Performance Test (5C-CPT) when the attentional load was increased. Neuropharmacology 2012, 62(3):1432-1441.
43. Young J.W., Powell S.B., Scott C.N., Zhou X., Geyer M.A. The effect of reduced dopamine D4 receptor expression in the 5-choice continuous performance task: separating response inhibition from premature responding. Behavioural Brain Research 2011, 222:183-192.
44. Green D.M., Swets J.A. Signal detection theory and psychophysics 1966, Wiley & Sons, New York.
45. McNicol D. A primer of signal detection theory 1972, George Allen & Unwin, London.
46. Frey P.W., Colliver J.A. Sensitivity and responsibility measures for discrimination learning. Learning and Motivation 1973, 4:327-342.
47. Marston H.M. Analysis of cognitive function in animals, the value of SDT. Brain Research. Cognitive Brain Research 1996, 3:269-277.
48. Sahgal A. Some limitations of indices derived from signal detection theory: evaluation of an alternative index for measuring bias in memory tasks. Psychopharmacology (Berlin) 1987, 91:517-520.
49. Hahn B., Shoaib M., Stolerman I.P. Nicotine-induced enhancement of attention in the five-choice serial reaction time task: the influence of task demands. Psychopharmacology (Berlin) 2002, 162:129-137.
50. Grottick A.J., Higgins G.A. Effect of subtype selective nicotinic compounds on attention as assessed by the five-choice serial reaction time task. Behavioural Brain Research 2000, 117:197-208.
51. Hahn B., Sharples C.G., Wonnacott S., Shoaib M., Stolerman I.P. Attentional effects of nicotinic agonists in rats. Neuropharmacology 2003, 44:1054-1067.
52. Young J.W., Crawford N., Kelly J.S., Kerr L.E., Marston H.M., Spratt C., et al. Impaired attention is central to the cognitive deficits observed in alpha 7 deficient mice. European Neuropsychopharmacology 2007, 17:145-155.
53. Hoyle E., Genn R.F., Fernandes C., Stolerman I.P. Impaired performance of alpha7 nicotinic receptor knockout mice in the five-choice serial reaction time task. Psychopharmacology (Berlin) 2006, 189:211-223.
54. Shrout P.E. Measurement reliability and agreement in psychiatry. Statistical Methods in Medical Research 1998, 7:301-317.
55. Ellis J.R., Ellis K.A., Bartholomeusz C.F., Harrison B.J., Wesnes K.A., Erskine F.F., et al. Muscarinic and nicotinic receptors synergistically modulate working memory and attention in humans. International Journal of Neuropsychopharmacology 2006, 9:175-189.
56. Wesnes K., Revell A. The separate and combined effects of scopolamine and nicotine on human information processing. Psychopharmacology (Berlin) 1984, 84:5-11.
57. Floresco S.B., Geyer M.A., Gold L.H., Grace A.A. Developing predictive animal models and establishing a preclinical trials network for assessing treatment effects on cognition in schizophrenia. Schizophrenia Bulletin 2005, 31:888-894.
58. Jones D.N.C., Garlton J.E., Minassian A., Perry W., Geyer M.A. Developing new drugs for schizophrenia: from animals to the clinic. Animal and translational models for CNS drug discovery: psychiatric disorders 2008, 199-262. Elsevier Inc., New York. R. McArthur, F. Borsini (Eds.).
59. Young J.W., Zhou X., Geyer M.A. Animal models of schizophrenia. Behavioral neurobiology of schiozphrenia and tis treatment 2010, 391-433. Springer, Berlin. N.R. Swerdlow (Ed.).
60. Howe W.M., Ji J., Parikh V., Williams S., Mocaer E., Trocme-Thibierge C., et al. Enhancement of attentional performance by selective stimulation of alpha4beta2* nAChRs: underlying cholinergic mechanisms. Neuropsychopharmacology 2010, 35:1391-1401.
61. Sarter M., Parikh V., Howe W.M. nAChR agonist-induced cognition enhancement: integration of cognitive and neuronal mechanisms. Biochemical Pharmacology 2009, 78:658-667.
62. McGaughy J., Decker M.W., Sarter M. Enhancement of sustained attention performance by the nicotinic acetylcholine receptor agonist ABT-418 in intact but not basal forebrain-lesioned rats. Psychopharmacology (Berlin) 1999, 144:175-182.
63. Turchi J., Holley L.A., Sarter M. Effects of nicotinic acetylcholine receptor ligands on behavioral vigilance in rats. Psychopharmacology (Berlin) 1995, 118:195-205.
64. Dudchenko P., Paul B., Sarter M. Dissociation between the effects of benzodiazepine receptor agonists on behavioral vigilance and responsitivity. Psychopharmacology (Berlin) 1992, 109:203-211.
65. Freedman R., Olincy A., Buchanan R.W., Harris J.G., Gold J.M., Johnson L., et al. Initial phase 2 trial of a nicotinic agonist in schizophrenia. American Journal of Psychiatry 2008, 165:1040-1047.
66. Grottick A.J., Haman M., Wyler R., Higgins G.A. Reversal of a vigilance decrement in the aged rat by subtype-selective nicotinic ligands. Neuropsychopharmacology 2003, 28:880-887.
67. Young J.W., Powell S.B., Geyer M.A. Mouse pharmacological models of cognitive disruption relevant to schizophrenia. Neuropharmacology 2012, 62:1381-1390.
68. McLean S.L., Grayson B., Idris N.F., Lesage A.S., Pemberton D.J., Mackie C., et al. Activation of alpha7 nicotinic receptors improves phencyclidine-induced deficits in cognitive tasks in rats: implications for therapy of cognitive dysfunction in schizophrenia. European Neuropsychopharmacology 2011, 21:333-343.
69. Rushforth S.L., Allison C., Wonnacott S., Shoaib M. Subtype-selective nicotinic agonists enhance olfactory working memory in normal rats: a novel use of the odour span task. Neuroscience Letters 2010, 471:114-118.
70. Young J.W., Meves J.M., Tarantino I.S., Caldwell S., Geyer M.A. Delayed procedural learning in alpha7-nicotinic acetylcholine receptor knockout mice. Genes, Brain, and Behavior 2011, 10:720-733.
71. Malysz J., Anderson D.J., Gronlien J.H., Ji J., Bunnelle W.H., Hakerud M., et al. In vitro pharmacological characterization of a novel selective alpha7 neuronal nicotinic acetylcholine receptor agonist ABT-107. Journal of Pharmacology and Experimental Therapeutics 2010, 334:863-874.
72. Othman A.A., Lenz R.A., Zhang J., Li J., Awni W.M., Dutta S. Single- and multiple-dose pharmacokinetics, safety, and tolerability of the selective alpha7 neuronal nicotinic receptor agonist, ABT-107, in healthy human volunteers. Journal of Clinical Pharmacology 2011, 51:512-526.
73. Thomsen M.S., Christensen D.Z., Hansen H.H., Redrobe J.P., Mikkelsen J.D. Alpha(7) nicotinic acetylcholine receptor activation prevents behavioral and molecular changes induced by repeated phencyclidine treatment. Neuropharmacology 2009, 56:1001-1009.
74. Turek J.W., Kang C.H., Campbell J.E., Arneric S.P., Sullivan J.P. A sensitive technique for the detection of the alpha 7 neuronal nicotinic acetylcholine receptor antagonist, methyllycaconitine, in rat plasma and brain. Journal of Neuroscience Methods 1995, 61:113-118.
75. Cilia J., Cluderay J.E., Robbins M.J., Reavill C., Southam E., Kew J.N., et al. Reversal of isolation-rearing-induced PPI deficits by an alpha7 nicotinic receptor agonist. Psychopharmacology (Berlin) 2005, 182:214-219.
76. Levin E.D. Alpha7-nicotinic receptors and cognition. Current Drug Targets 2012, 13:602-606.
77. Duka T., Ott H., Rohloff A., Voet B. The effects of a benzodiazepine receptor antagonist beta-carboline ZK-93426 on scopolamine-induced impairment on attention, memory and psychomotor skills. Psychopharmacology (Berlin) 1996, 123:361-373.
78. Young J.W., Geyer M.A., Rissling A.J., Eyler L.T., Asgaard G.L., Light G.A. Impaired vigilance but not accuracy of patients with schziophrenia in a human version of the rodent 5-choice continuous performance test. Schizophrenia Bulletin 2011, 37:236.
79. Jones D.N., Higgins G.A. Effect of scopolamine on visual attention in rats. Psychopharmacology (Berlin) 1995, 120:142-149.