Performance of α7 nicotinic receptor null mutants is impaired in appetitive learning measured in a signaled nose poke task

Behavioural Brain Research

Volumn 162, Issue 1, 2005, Pages 143-152

  Keller, Jason J ^a   Keller, Ashleigh B ^a   Bowers, Barbara J ^a   Wehner, Jeanne M ^a,b  

^a UNIVERSITY OF COLORADO   (United States)

^b UNIVERSITY OF COLORADO   (United States)

Author keywords

Impulsivity; Learning and memory; Mutant mice; Nicotinic receptors

Indexed keywords

NICOTINIC RECEPTOR; NICOTINIC RECEPTOR ALPHA 5; NICOTINIC RECEPTOR ALPHA 7; NICOTINIC RECEPTOR BETA 2; NICOTINIC RECEPTOR BETA 3; NICOTINIC RECEPTOR BETA 4; SUCROSE; UNCLASSIFIED DRUG; ALPHA-BUNGAROTOXIN RECEPTOR; BUNGAROTOXIN RECEPTOR;

ANIMAL EXPERIMENT; ARTICLE; AUDITORY STIMULATION; BEHAVIOR; COMPARATIVE STUDY; CONDITIONED REFLEX; CONTROLLED STUDY; FEMALE; GENE MUTATION; IMPULSIVENESS; LEARNING; MALE; MEMORY; MENTAL TASK; MOUSE; MOUSE MUTANT; NONHUMAN; NOSE; PRIORITY JOURNAL; PROTEIN FUNCTION; RESPONSE TIME; REWARD; TASK PERFORMANCE; TRAINING; WILD TYPE; ANALYSIS OF VARIANCE; ANIMAL; ANIMAL BEHAVIOR; APPETITE; C57BL MOUSE; GENETICS; LEARNING DISORDER; PATHOPHYSIOLOGY; PHYSIOLOGY; PSYCHOMOTOR PERFORMANCE; REINFORCEMENT; TIME;

ANALYSIS OF VARIANCE; ANIMALS; APPETITIVE BEHAVIOR; BEHAVIOR, ANIMAL; LEARNING DISORDERS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PSYCHOMOTOR PERFORMANCE; RECEPTORS, NICOTINIC; REINFORCEMENT (PSYCHOLOGY); REINFORCEMENT SCHEDULE; TIME FACTORS;

EID: 19444368101     PISSN: 01664328     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbr.2005.03.004     Document Type: Article

References (73)

1. C.E. Adams, J.A. Stitzel, A.C. Collins, and R. Freedman α7-Nicotinic receptor expression and the anatomical organization of hippocampal interneurons Brain Res 922 2001 180 190
2. C.E. Adams Comparisons of α7 nicotinic acetylcholine receptor development in the hippocampal formation of C3H and DBA/2 mice Dev Brain Res 143 2003 137 149
3. N.A. Addy, A. Nakijama, and E.D. Levin Nicotinic mechanisms of memory: effects of acute local DHBE and MLA infusions in the basolateral amygdala Cogn Brain Res 16 2003 51 57
4. M. Alkondon, E.F. Pereira, C.T. Barbosa, and E.X. Albuquerque Neuronal nicotinic acetylcholine receptor activation modulates gamma-aminobutyric acid release from CA1 neurons of rat hippocampal slices J Pharmacol Exp Ther 283 1997 1396 1411
5. L. Azam, U. Winzer-Sherman, and F.M. Leslie Co-rxpression of α7 and β2 nicotinic acetylcholine receptor subunit mRNAs with rat brain cholinergic neurons Neuroscience 119 2003 965 977
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. A. Blondel, D.J. Sanger, and P.C. Moser Characterisation of the effects of nicotine in the five-choice serial reaction time task in rats: antagonist studies Psychopharmacology 149 2000 293 305
8. B.J. Bowers, and J.M. Wehner Ethanol consumption and behavioral impulsivity are increased in protein kinase Cγ null mutant mice J Neurosci 21 2001 RC180
9. B.J. Bowers, T.D. McClure-Begley, J.J. Keller, R. Paylor, A.C. Collins, and J.M. Wehner Deletion of the α7 nicotinic receptor subunit gene results in increased sensitivity to several behavioral effects produced by alcohol Alcoholism: Clin Exp Res 29 2005 295 302
10. A.E. Bullock, B.S. Slobe, V. Vazquez, and A.C. Collins Inbred mouse strains differ in the regulation of startle and prepulse inhibition of the startle response Behav Neurosci 111 1997 1353 1360
11. B.J. Caldarone, C.H. Duman, and M.R. Picciotto Fear conditioning and latent inhibition in mice lacking the high affinity subclass of nicotinic acetylcholine receptors in the brain Neuropharmacology 39 2000 2779 2784
12. Y. Chudasama, F. Passetti, Rhodes SEV, D. Lopian, A. Desai, and T.W. Robbins Dissociable aspects of performance on the 5-choice serial reaction time task following lesions of the dorsal anterior cingulate, infralimbic and orbitofrontal cortex in the rat: differential effects on selectivity, impulsivity, and compulsivity Behav Brain Res 146 2003 105 119
13. C. Cui, T.K. Booker, R.S. Allen, S.R. Grady, P. Whiteaker, and M.J. Marks The beta3 receptor subunit: a component of the alpha-conotoxin MII binding nAChRs which modulate dopamine release and related behaviors J Neurosci 23 2003 11045 11053
14. F. Dajas-Bailador, and S. Wonnacott Nicotinic acetylcholine receptors and the regulation of neuronal signalling Trends Pharm Sci 25 2004 317 324
15. K.Y. Dineley, M. Westerman, D. Bui, K. Bell, K.H. Ashe, and J.D. Sweatt β-Amyloid activated the mitogen-activated protein kinase cascade via hippocampal α7 nicotinic acetylcholine receptors: in vitro and in vivo mechanisms related to Alzheimer's disease J Neurosci 21 2001 4125 4133
16. K. Dineley-Miller, and J. Patrick Gene transcripts for the nicotinic acetylcholine receptor subunit, beta4, are distributed in multiple areas of the rat central nervous system. Mol Brain Res 16 1992 339 344
17. C.J. Frazier, Y.D. Rollins, C.R. Breese, S. Leonard, R. Freedman, and T.V. Dunwiddie Acetylcholine activates an alpha-bungarotoxin-sensitive nicotinic current in rat hippocampal interneurons, but not pyramidal cells J Neurosci 18 1998 1187 1195
18. R. Freedman, H. Coon, M. Myles-Worsley, A. Orr-Urteger, A. Olincy, and A. Davis Linkage of a neurophysiological deficit in schizophrenia to a chromosome 15 locus Proc Natl Acad Sci USA 94 1997 587 592
19. R. Freedman, M. Hall, L.E. Adler, and D. Leonard Evidence in postmortem brain tissue for decreased numbers of hippocampal nicotinic receptors in schizophrenia Biol Psychiatry 38 1995 22 33
20. L.C. Gahring, K. Persiyanov, D. Dunn, R. Wiess, E.L. Meyer, and S.W. Rogers Mouse strain-specific nicotinic receptor expression by inhibitory interneurons and astrocytes in the dorsal hippocampus J Comp Neurol 468 2004 334 346
21. D.G. Gilbert, and B.O. Gilbert Personality, psychopathology, and nicotine response as mediators of the genetics of smoking Behav Genet 25 1995 133 147
22. P.S. Goldman-Rakic The prefrontal landscape: implications of functional architecture for understanding human mentation and the central executive Philos Trans R Soc Lond B Biol Sci 29 351 1996 1445 1453
23. T.J. Gould, A.C. Collins, and J.M. Wehner Nicotine enhances latent inhibition and ameliorates ethanol-induced deficits in latent inhibition Nicotine Tob Res 3 2001 17 24
24. T.J. Gould, and J.S. Higgins Nicotine enhances contextual fear conditioning in C57BL/6J mice at 1 and 7 days post-training Neurobiol Learn Mem 80 2003 147 157
25. T.J. Gould, and J.A. Lommock Nicotine enhances contextual fear conditioning and ameliorates ethanol-induced deficits in contextual fear conditioning Behav Neurosci 117 2003 1276 1282
26. T.J. Gould, and J.M. Wehner Nicotine enhancement of contextual fear conditioning Behav Brain Res 102 1999 31 39
27. S. Granon, P. Faure, and J.P. Changeux Executive and social behaviors under nicotinic receptor regulation. Proc Natl Acad Sci USA 100 2003 9596 9601
28. A.J. Grottick, and G.A. Higgins Effect of subtype selective nicotinic compounds on attention as assessed by the five-choice serial reaction time task Behav Brain Res 117 2000 197 208
29. B. Hahn, C.G.V. Sharples, S. Wonnacott, M. Shoaib, and I.P. Stolerman Attentional effects of nicotinic agonists in rats Neuropharmacology 44 2003 1054 1067
30. B. Hahn, M. Shoaib, and I.P. Stolerman Involvement of the prefrontal cortex but not the dorsal hippocampus in the attention-enhancing effects of nicotine in rats Psychopharmacology 16 2003 16
31. J.G. Harris, D. Allenswroth, L. Martin, J. Tregellas, B. Sullivan, and G. Zerbe Effects of nicotine on cognitive deficits in schizophrenia Neuropsychopharmacology 29 2004 1378 1385
32. S.C. Harvey, and C.W. Luetje Determinants of competitive antagonist sensitivity on neuronal nicotinic receptor beta subunits J Neurosci 16 1996 3798 3806
33. S.L. King, M.J. Marks, S.R. Grady, B.J. Caldarone, A.O. Koren, and A.G. Mukhin Conditional expression in corticothalamic efferents reveals a developmental role for nicotinic acetylcholine receptors in modulation of passive avoidance behavior J Neurosci 23 2003 3837 3843
34. R. Klink, A. de Kerchove d'Exaerde, M. Zoli, and J.P. Changeux Molecular and physiological diversity of nicotinic acetylcholine receptors in the midbrain dopaminergic nuclei J Neurosci 21 2001 1452 1463
35. S.R. Laviolette, and D. van der Kooy The neurobiology of nicotine addiction: bridging the gap from molecules to behavior Nat Rev Neurosci 5 2004 55 65
36. 2+ ions in nicotinic facilitation of GABA release in mouse thalamus J Neurosci 17 1997 576 585
37. S. Leonard, J. Gault, J. Hopkins, J. Logel, R. Vianzon, and M. Short Association of promoter variants in the α7 nicotinic acetylcholine receptor subunit gene with an inhibitory deficit found in schizophrenia Arch Gen Psychiatry 59 2002 1085 1096
38. E.D. Levin Nicotinic receptor subtypes and cognitive function J Neurobiol 53 2002 633 640
39. E.D. Levin, A. Bradley, N. Addy, and N. Sigurani Hippocampal alpha 7 and alpha 4 beta 2 nicotinic receptors and working memory Neuroscience 109 2000 757 765
40. E.D. Levin, and B.B. Simon Nicotinic acetylcholine involvement in cognitive function in animals Psychopharmacology (Berl) 138 1998 217 230
41. J. Lindstrom, R. Anand, X. Peng, V. Gerzanich, F. Wang, and Y. Li Neuronal nicotinic receptor subtypes Ann NY Acad Sci 757 1995 100 116
42. S.F. Logue, R.J. Swartz, and J.M. Wehner Genetic correlation between performance on an appetitive-signaled nosepoke task and voluntary ethanol consumption Alcohol Clin Exp Res 22 1998 1912 1920
43. M.J. Marks, J.R. Pauly, S.D. Gross, E.S. Deneris, I. Hermans-Borgmeyer, and S.F. Heinemann Nicotine binding and nicotinic receptor subunit RNA after chronic nicotine treatment J Neurosci 12 1992 2765 2784
44. D.S. McGehee, M.J. Heath, S. Gelber, P. Devay, and L.W. Role Nicotine enhancement of fast excitatory synaptic transmission in CNS by presynaptic receptors Science 269 1995 1692 1696
45. L.A. Miner, M. Ostrander, and M. Sarter Effects of ibotenic acid-induced loss of neurons in the medial prefrontal cortex of rats on behavioral vigilance: evidence for executive dysfunction J Psychopharmacol 11 1997 169 178
46. N.R. Mirza, and I.P. Stolerman Nicotine enhances sustained attention in the rat under specific conditions Psychopharmacology 138 1998 266 274
47. S.H. Mitchell Measures of impulsivity in cigarette smokers and non-smokers Psychopharmacology 146 1999 455 464
48. A.J. Mogg, P. Whiteaker, J.M. McIntosh, M. Marks, A.C. Collins, and S. Wonnacott Methyllycaconitine is a potent antagonist of alpha-conotoxin-MII- sensitive presynaptic nicotinic acetylcholine receptors in rat striatum J Pharmacol Exp Ther 302 2002 197 204
49. D.S. Olton, G.L. Wenk, R.M. Church, and W.H. Meck Attention and the frontal cortex as examined by simultaneous temporal processing Neuropsychologia 26 1998 307 318
50. A. Orr-Urtreger, F.M. Goldner, M. Seaki, I. Lorenzo, L. Goldberg, and M. DeBiasi Mice deficient in the alpha7 neuronal nicotinic acetylcholine receptor lack alpha-bungarotoxin binding sites and hippocampal fast nicotinic currents J Neurosci 17 1997 9165 9171
51. J.R. Pauly, M.J. Marks, S.D. Gross, and A.C. Collins An autoradiographic analysis of cholinergic receptors in mouse brain after chronic nicotine treatment J Pharmacol Exp Ther 258 1991 1127 1136
52. R. Paylor, M. Nguyen, J.N. Crawley, J. Patrick, A. Beaudet, and A. Orr-Urtereger α7-Nicotinic receptor subunits are not necessary for hippocampal-dependent learning or sensorimotor gating: a behavioral characterization of Acra7-deficient mice Learn Mem 5 1998 302 316
53. M.R. Picciotto, B.J. Caldarone, D.H. Brunzell, V. Zachariou, T.R. Stevens, and S.L. King Neuronal nicotinic acetylcholine receptor subunit knockout mice: physiological and behavioral phenotypes and possible clinical implications Pharmacol Ther 92 2001 89 108
54. M.R. Picciotto, and W.A. Corrigall Neuronal systems underlying behaviors related to nicotine addiction: neural circuits and molecular genetics J Neurosci 22 2002 3338 3341
55. M.R. Picciotto, M. Zoli, C. Lena, A. Bessis, Y. Lallemand, and N. LeNovere Abnormal avoidance learning in mice lacking functional high-affinity nicotine receptor in the brain Nature 374 1995 65 67
56. F. Pissetti, Y. Chudasama, and T.W. Robbins The frontal cortex of the rat and visual attentional performance: dissociable functions of distinct medial prefrontal subregions Cereb Cortex 12 2002 1254 1268
57. K.A. Radcliffe, and J.A. Dani Nicotinic stimulation produces multiple forms of increased glutamatergic synaptic transmission J Neurosci 18 1998 7075 7083
58. R. Salas, A. Orr-Urtreger, R.S. Broide, A. Beaudet, R. Paylor, and M. De Biasi The nicotinic acetylcholine receptor subunit alpha5 mediates short-term effects of nicotine in vivo Mol Pharmacol 63 2003 1059 1066
59. O. Salminen, K.L. Murphy, J.M. McIntosh, J. Drago, M.J. Marks, and A.C. Collins Subunit composition and pharmacology of two classes of striatal presynaptic nicotinic acetylcholine receptors mediating dopamine release in mice Mol Pharmacol 65 2004 1526 1535
60. B. Shilstrom, M.V. Fagerquist, X. Zhang, P. Hertel, G. Panagis, and G.G. Nomikos Putative role of presynatic α7* nicotinic receptors in nicotine stimulated increases in extracellular levels of glutamate and aspartate in the ventral tegmental area Synapse 38 2000 375 383
61. B. Schilstrom, H.M. Svensson, T.H. Svensson, and G.G. Nomikos Nicotine and food-induced dopamine release in the nucleus accumbens of the rat: putative role of α7 nicotinic receptors in the ventral tegmental area Neuroscience 85 1998 1005 1009
62. M. Shoaib, J. Gommans, A. Morley, I.P. Stolerman, R. Grailhe, and J.P. Changeux The role of nicotinic receptor beta-2 subunits in nicotine discrimination and conditioned taste aversion Neuropharmacology 42 2002 530 539
63. K.E. Stevens, R. Freedman, A.C. Collins, M. Hall, S. Leonard, and M.J. Marks Genetic correlation of inhibitory gating of hippocampal auditory evoked response and alpha-bungarotoxin-binding nicotinic cholinergic receptors in inbred mouse strains Neuropsychopharmacology 15 1996 152 162
64. J.E. Steinmetz, S.F. Logue, and D.P. Miller Using signaled barpressing tasks to study the neural substrates of appetitive and aversive learning in rats: behavioral manipulations and cerebellar lesions Behav Neurosci 107 1993 941 954
65. I.P. Stolerman, N.R. Mirza, B. Hahn, and M. Shoaib Nicotine in an animal model of attention Eur J Pharmacol 393 2000 147 154
66. E. Wada, K. Wada, J. Boulter, E. Deneris, S. Heinemann, and J. Patrick Distribution of alpha 2, alpha 3, alpha 4, and beta 2 neuronal nicotinic receptor subunit mRNAs in the central nervous system: a hybridization histochemical study in the rat J Comp Neurol 284 1989 314 335
67. J.M. Wehner, J.J. Keller, A.B. Keller, M.R. Picciotto, R. Paylor, and J.K. Booker Role of neuronal nicotinic receptors in the effects of nicotine and ethanol on contextual fear conditioning Neuroscience 129 2004 11 24
68. D.R. Weinberger, M.F. Egan, A. Bertolino, J.H. Callicott, V.S. Mattay, and B.K. Lipska Neurobiology of schizophrenia and the role of atypical antipsychotics Biol Pyschiatry 50 2001 825 844
69. P. Whiteaker, A.R. Davies, M.J. Marks, I.S. Blagbrough, B.V. Potter, and A.J. Wolstenholme An autoradiographic study of the distribution of binding sites for the novel alpha7-selective nicotinic radioligand [3H]-methyllycaconitine in the mouse brain Eur J Neurosci 11 1999 2689 2696
70. P. Whiteaker, C.G. Peterson, W. Xu, J.M. McIntosh, R. Paylor, and A.L. Beaudet Involvement of the alpha 3 subunit in central nicotinic binding populations J Nueurosci 22 2002 2522 2529
71. S. Wonnacott Presynaptic nicotinic ACh receptors Trends Neurosci 20 1997 92 98
72. W. Xu, A. Orr-Urtreger, F. Nigro, S. Gelber, C.B. Sutcliffe, and D. Armstrong Multiorgan autonomic dysfunction in mice lacking the beta2 and the beta4 subunits of neuronal nicotinic acetylcholine receptors J Neurosci 19 1999 9298 9305
73. J.W. Young, K. Finlayson, C. Spratt, H.M. Marston, N. Crawford, and J.S. Kelly Nicotine improves sustained attention in mice: evidence for involvement of the α7 nicotinic acetylcholine receptor Neuropsychopharmacology 29 2004 891 900