Olfactory discrimination varies in mice with different levels of α7-nicotinic acetylcholine receptor expression

Brain Research

Volumn 1358, Issue , 2010, Pages 140-150

  Hellier, Jennifer L ^a,b   Arevalo, Nicole L ^a,b   Blatner, Megan J ^a,b   Dang, An K ^a,b   Clevenger, Amy C ^a,b   Adams, Catherine E ^b,c   Restrepo, Diego ^a,b  

^a UNIVERSITY OF COLORADO   (United States)

^b UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

bungarotoxin; 7 nACh; Behavior; MLPEST; Odor discrimination; Olfaction

Indexed keywords

ALPHA 7 NICOTINIC ACETYLCHOLINE RECEPTOR; ALPHA BUNGAROTOXIN I 125; NICOTINIC RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTORADIOGRAPHY; BEHAVIOR; KNOCKOUT GENE; MOUSE; MOUSE STRAIN; NONHUMAN; OLFACTORY BULB; OLFACTORY DISCRIMINATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SMELLING; ZONA GLOMERULOSA;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN; BUNGAROTOXINS; DISCRIMINATION (PSYCHOLOGY); IODINE ISOTOPES; MICE; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, KNOCKOUT; ODORS; OLFACTORY PATHWAYS; PROTEIN BINDING; REACTION TIME; RECEPTORS, NICOTINIC; SMELL;

MUS;

EID: 77957351764     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2010.08.027     Document Type: Article

References (89)

1. C.E. Adams, J.C. Yoncheck, L. Zheng, A.C. Collins, and K.E. Stevens Altered hippocampal circuit function in C3H α7 null mutant heterozygous mice Brain Res. 1194 2008 138 145
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 (Pubitemid 23356580)
3. H. Akil, S. Brenner, E. Kandel, K.S. Kendler, M.C. King, E. Scolnick, J.D. Watson, and H.Y. Zoghbi Medicine. The future of psychiatric research: genomes and neural circuits Science 327 2010 1580 1581
4. E.X. Albuquerque, E.F. Pereira, N.G. Castro, M. Alkondon, S. Reinhardt, H. Schröder, and A. Maelicke Nicotinic receptor function in the mammalian central nervous system Ann. N.Y. Acad. Sci. 757 1995 48 72
5. E.X. Albuquerque, E.F. Pereira, M. Alkondon, and S.W. Rogers Mammalian nicotinic acetylcholine receptors: from structure to function Physiol. Rev. 89 2009 73 120
6. M. Alkondon, E.S. Rocha, A. Maelicke, and E.X. Albuquerque Diversity of nicotinic acetylcholine receptors in rat brain. V. alpha-bungarotoxin-sensitive nicotinic receptors in olfactory bulb neurons and presynaptic modulation of glutamate release J. Pharmacol. Exp. Ther. 278 1996 1460 1471
7. A.J. Apter, J.F. Gent, and M.E. Frank Fluctuating olfactory sensitivity and distorted odor perception in allergic rhinitis Arch. Otolaryngol. Head Neck Surg. 125 1999 1005 1010
8. S.E. Arnold, L.Y. Han, P.J. Moberg, B.I. Turetsky, R.E. Gur, J.Q. Trojanowski, and C.G. Hahn Dysregulation of olfactory receptor neuron lineage in schizophrenia Arch. Gen. Psychiatry 58 2001 829 835
9. B. Atanasova, J. Graux, W. El Hage, C. Hommet, V. Camus, and C. Belzung Olfaction: a potential cognitive marker of psychiatric disorders Neurosci. Biobehav. Rev. 32 2008 1315 1325
10. J.L. Aungst, P.M. Heyward, A.C. Puche, S.V. Karnup, A. Hayar, G. Szabo, and M.T. Shipley Centre-surround inhibition among olfactory bulb glomeruli Nature 426 2003 623 629
11. H. Baker, and A.I. Farbman Olfactory afferent regulation of the dopamine phenotype in the fetal rat olfactory system Neuroscience 52 1 1993 115 134
12. D. Bhugra The global prevalence of schizophrenia PLoS Med. 2 2005 e151
13. N.P. Brooks, S. Mexal, and J.A. Stitzel Chrna7 genotype is linked with alpha7 nicotinic expression but not alpha7 RNA levels Brain Res. 1263 2009 1 9
14. J.J. Buccafusco, S.R. Letchworth, M. Bencherif, and P.M. Lippiello Long-lasting cognitive improvement with nicotinic receptor agonists: mechanisms of pharmacokinetic-pharmacodynamic discordance Trends Pharmacol. Sci. 26 2005 352 360
15. W.S. Cain, J.F. Gent, F.A. Catalanotto, and R.B. Goodspeed Clinical evaluation of olfaction Am. J. Otolaryngol. 4 1983 252 256
16. D. Castle, S. Wessely, G. Der, and R.M. Murray The incidence of operationally defined schizophrenia in Camberwell, 1965-84 Br. J. Psychiatry 159 1991 790 794
17. J.W. Cave, and H. Baker Dopamine systems in the forebrain Adv. Exp. Med. Biol. 651 2009 15 35
18. T.A. Christensen, and J. White Representation of olfactory information in the brain T.E. Finger, D. Restrepo, W.L. Silver, Neurobiology of Taste and Smell 2000 John Wiley and Sons 201 232
19. A.C. Clevenger, and D. Restrepo Evaluation of the validity of a maximum likelihood adaptive staircase procedure for measurement of olfactory detection threshold in mice Chem. Senses 31 2006 9 26
20. J. Court, D. Spurden, S. Lloyd, I. McKeith, C. Ballard, N. Cairns, R. Kerwin, R. Perry, and E. Perry Neuronal nicotinic receptors in dementia with Lewy bodies and schizophrenia: alpha-bungarotoxin and nicotine binding in the thalamus J. Neurochem. 73 1999 1590 1597
21. F.B. Dickerson Women, aging, and schizophrenis J. Women Aging 19 2007 49 61
22. M.L. Doop, and S. Park On knowing and judging smells: identification and hedonic judgment of odors in schizophrenia Schizophr. Res. 81 2006 317 319
23. R.L. Doty, R. Bagla, and N. Kim Physostigmine enhances performance on an odor mixture discrimination test Physiol. Behav. 65 1999 801 804
24. W. Doucette, J. Milder, and D. Restrepo Adrenergic modulation of olfactory bulb circuitry affects odor discrimination Learn. Mem. 14 2007 539 547
25. R.C. Drisdel, and W.N. Green Neuronal alpha-bungarotoxin receptors are alpha7 subunit homomers J. Neurosci. 20 2000 133 139
26. T.P. Dunn, and M.P. Weller Olfaction in schizophrenia Percept. Mot. Skills 69 1989 833 834
27. A.B. Elgoyhen, D.E. Vetter, E. Katz, C.V. Rothlin, S.F. Heinemann, and J. Boulter Alpha10: a determinant of nicotinic cholinergic receptor function in mammalian vestibular and cochlear mechanosensory hair cells PNAS 98 2001 3501 3506
28. D. Franceschini, R. Paylor, R. Broide, R. Salas, L. Bassetto, C. Gotti, and M. De Biasi Absence of alpha7-containing neuronal nicotinic acetylcholine receptors does not prevent nicotine-induced seizures Brain Res. Mol. Brain Res. 98 2002 29 40
29. 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
30. R. Freedman, H. Coon, M. Myles-Worsley, A. Orr-Urtreger, A. Olincy, A. Davis, M. Polymeropoulos, J. Holik, J. Hopkins, M. Hoff, J. Rosenthall, M.C. Waldo, F. Reimherr, P. Wender, J. Yaw, D.A. Young, C.R. Breese, C. Adams, D. Patternson, L.E. Adler, L. Kyuglyak, S. Leonard, and W. Byerley Linkage of a neurophysiological deficit in schizophrenia to a chromosome 15 locus PNAS 94 1997 587 592
31. R.E. Frye, B.S. Schwartz, and R.L. Doty Dose-related effects of cigarette smoking on olfactory function JAMA 263 1990 1233 1236
32. E.M. Goldner, L. Hsu, P. Waraich, and J.M. Somers Prevalence and incidence studies of schizophrenic disorders: a systematic review of the literature Can. J. Psychiatry 47 2002 833 843
33. I.I. Gottesman, and T.D. Gould The endophenotype concept is psychiatry: etymology and strategic intentions Am. J. Psychiatry 160 2003 636 645
34. T.D. Gould, and I.I. Gottesman Psychiatric endophenotypes and the development of valid animal models Genes Brain Behav. 5 2 2006 113 119
35. A. Graham, J.A. Court, C.M. Martin-Ruiz, E. Jaros, R. Perry, S.G. Volsen, S. Bose, N. Evans, P. Ince, A. Kuryatov, J. Lindstrom, C. Gotti, and E.K. Perry Immunohistochemical localization of nicotinic acetylcholine receptor subunits in human cerebellum Neuroscience 113 2002 493 507
36. 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
37. H.H. Hansen, D.B. Timmermann, D. Peters, C. Walters, M.I. Damaj, and J.D. Mikkelsen Alpha-7 nicotinic acetylcholine receptor agonists selectively activate limbic regions of the rat forebrain: an effect similar to antipsychotics J. Neurosci. Res. 85 2007 1810 1818
38. +-induced calcium responses in mouse olfactory receptor neurons in situ J. Neurophysiol. 91 2004 1492 1499
39. D.J. Houlihan, M. Flaum, S.E. Arnold, M. Keshaven, and R. Alliger Further evidence for olfactory identification deficits in schizophrenia Schizophr. Res. 12 1994 179 182
40. R.G. Isseroff, M. Stoler, D. Ophir, D. Lancet, and P. Sirota Olfactory sensitivity to androstenone in schizophrenic patients Biol. Psychiatry 22 1987 922 925
41. B.A. Johnson, H. Farahbod, S. Saber, and M. Leon Effects of functional group position on spatial representations of aliphatic odorants in the rat olfactory bulb J. Comp. Neurol. 483 2005 192 204
42. L.C. Kopala, C. Clark, and T. Hurwitz Olfactory deficits in neuroleptic naïve patients with schizophrenia Schizophr. Res. 8 1993 245 250
43. L. Kopala, K. Good, J. Martzke, and T. Hurwitz Olfactory deficits in schizophrenia are not a function of task complexity Schizophr. Res. 17 1995 195 199
44. J.C. Lauterborn, P.J. Isackson, R. Montalvo, and C.M. Gall In situ hybridization localization of choline acetyltransferase mRNA in adult rat brain and spinal cord Brain Res. Mol. Brain Res. 17 1993 59 69
45. H. Le Jeune, and F. Jourdan Postnatal development of cholinergic markers in the rat olfactory bulb: a histochemical and immunocytochemical study J. Comp. Neurol. 314 1991 383 395
46. H. Le Jeune, I. Aubert, F. Jourdan, and R. Quirion Comparative laminar distribution of various autoradiographic cholinergic markers in adult rat main olfactory bulb J. Chem. Neuroanat. 9 1995 99 112
47. H. Le Jeune, I. Aubert, F. Jourdan, and R. Quirion Developmental profiles of various cholinergic markers in the rat main olfactory bulb using quantitative autoradiography J. Comp. Neurol. 373 1996 433 450
48. S. Leonard, and D. Bertrand Neuronal nicotinic receptors: from structure to function Nicotine Tob. Res. 3 2001 203 223 (Pubitemid 32821649)
49. 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
50. M.R. Linschoten, L.O. Harvey Jr, P.M. Eller, and B.W. Jafek Fast and accurate measurement of taste and smell thresholds using a maximum-likelihood adaptive staircase procedure Percept. Psychophys. 63 2001 1330 1347
51. C. Linster, P.A. Garcia, M.E. Hasselmo, and M.G. Baxter Selective loss of cholinergic neurons projecting to the olfactory system increases perceptual generalization between similar, but not dissimilar, odorants Behav. Neurosci. 115 2001 826 833
52. D. Malaspina, A.D. Wray, J.H. Friedman, X. Amador, S. Yale, A. Hasan, J.M. Gorman, and C.A. Kaufmann Odor discrimination deficits in schizophrenia: association with eye movement dysfunction J. Neuropsychiatry Clin. Neurosci. 6 1994 273 278
53. D. Malaspina, E. Coleman, R.R. Goetz, J. Harkavy-Friedman, C. Corcoran, X. Amador, S. Yale, and J.M. Gorman Odor identification, eye tracking and deficit syndrome schizophrenia Biol. Psychiatry 51 2002 809 815
54. M.J. Marks, E. Romm, S.M. Campbell, and A.C. Collins Variation of nicotinic binding sites among inbred strains Pharmacol. Biochem. Behav. 33 1989 679 689
55. M.J. Marks, J.R. Pauly, E.U. Grun, and A.C. Collins ST/b and DBA/2 mice differ in brain α-bungarotoxin binging and α7 nicotinic receptor subunit mRNA levels: a quantitative autoradiographic analysis Mol. Brain Res. 39 1996 207 222
56. A. Marutle, X. Zhang, J. Court, M. Piggott, M. Johnson, R. Perry, E. Perry, and A. Nordberg Laminar distribution of nicotinic receptor subtypes in cortical regions in schizophrenia J. Chem. Neuroanat. 22 2001 115 126
57. P.J. Moberg, S.E. Arnold, R.L. Doty, C. Kohler, S. Kanes, S. Seigel, R.E. Gur, and B.I. Turestsky Impairment of odor hedonics in men with schizophrenia Am. J. Psychiatry 160 2003 1784 1789
58. P.J. Moberg, S.E. Arnold, R.L. Doty, R.E. Gur, C.C. Balderston, D.R. Roalf, R.C. Gur, C.G. Kohler, S.J. Kanes, S.J. Siegel, and B.I. Turetsky Olfactory functioning in schizophrenia: relationship to clinical, neuropsychological, and volumetric MRI measures J. Clin. Exp. Neuropsychol. 28 2006 1444 1461
59. T. Nagatsu, M. Levitt, and S. Udenfriend Tyrosine hydroxylase: the initial step in norepinephrine biosynthesis J. Biol. Chem. 239 1964 2910 2917
60. A.M. Oliva, E. Salcedo, J.L. Hellier, X. Ly, K. Koka, D.J. Tollin, and D. Restrepo Toward a mouse neuroethology in the laboratory environment PLoS ONE 5 6 2010 e11359 10.1371/journal.pone.0011359
61. R. Paylor, M. Nguyen, J.N. Crawley, J. Patrick, A. Beaudet, and A. Orr-Urtreger Alpha7 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
62. C.I. Rupp, W.W. Fleischhacker, G. Kemmler, C. Kremser, R.M. Bilder, S. Mechtcheriakov, P.R. Szeszko, T. Walch, M. Klimbacher, C. Maier, G. Albrecht, T. Lechner-Schoner, S. Felber, and H. Hinterhuber Olfactory functions and volumetric measures of orbitofrontal and limbic regions in schizophrenia Schizophr. Res. 74 2005 149 161
63. C.I. Rupp, W.W. Fleischhacker, G. Kemmler, H. Oberbauer, A.W. Scholtz, C. Wanko, and H. Hinterhuber Various bilateral olfactory deficits in male patients with schizophrenia Schizophr. Bull. 31 2005 155 165
64. M.L. Schaefer, D.A. Young, and D. Restrepo Olfactory fingerprints for major histocompatibility complex-determined body odors J. Neurosci. 21 2001 2481 2487
65. M.L. Schaefer, T.E. Finger, and D. Restrepo Variability of position of the P2 glomerulus within a map of the mouse olfactory bulb J. Comp. Neurol. 436 2001 351 362
66. P. Seguela, J. Wadiche, K. Dineley-Miller, J.A. Dani, and J.W. Patrick Molecular cloning, functional properties, and distribution of rat brain alpha 7: a nicotinic cation channel highly permeable to calcium J. Neurosci. 13 1993 596 604
67. M. Serby, P. Larsom, and D. Kalkstein Olfactory sense in psychoses Biol. Psychiatry 28 1990 830
68. L. Serova, and E.L. Sabban Involvement of α7 nicotinic acetylcholine receptors in gene expression of dopamine biosynthetic enzymes in rat brain J. Pharm. Expert. Ther. 303 2002 896 903
69. J.K. Simosky, K.E. Stevens, W.R. Kem, and R. Freedman Intragastric DMXB-A, an alpha7 nicotinic agonist, improves deficient sensory inhibition in DBA/2 mice Biol. Psychiatry 50 2001 493 500
70. B. Slotnick, and D. Restrepo Olfactometry with mice Curr. Protoc. Neorosci. 2005 8.20.1-8.20.24
71. K.E. Stevens, R. Freedman, A.C. Collins, M. Hall, S. Leonard, M.J. Marks, and G.M. Rose 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
72. R.J. Stevenson Perceptual learning with odors: implications for psychological accounts of odor quality perception Psychon. Bull. Rev. 8 2001 708 712
73. M. Stopfer, S. Bhagavan, B.H. Smith, and G. Laurent Impaired odour discrimination on desynchronization of odour-encoding neural assemblies Nature 390 1997 70 74
74. S. Takagi Degeneration and regeneration of the sensory neuron: studies on the olfactory epithelium Shinkei Kenkyu No Shimpo 13 1969 152 163
75. M.S. Thomsen, J.D. Mikkelsen, D.B. Timmermann, D. Peters, A. Hay-Schmidt, H. Martens, and H.H. Hansen The selective alpha7 nicotinic acetylcholine receptor agonist A-582941 activates immediate early genes in limbic regions of the forebrain: differential effects in the juvenile and adult rat Neuroscience 154 2008 741 753
76. M.S. Thomsen, A. Hay-Schmidt, H.H. Hansen, and J.D. Mikkelsen Distinct neural pathways mediate alpha7 nicotinic acetylcholine receptor-dependent activation of the forebrain Cereb. Cortex 2010 20 (9), 2092-2102
77. V. Tucci, A. Hardy, and P.M. Nolan A comparison of psychological and behavioral parameters in C57BL/6J mice undergoing food or water restriction regimes Behav. Brain Res. 173 2006 22 29
78. B.I. Turetsky, and P.J. Moberg An odor-specific threshold deficit implicates abnormal intracellular cyclic AMP signaling in schizophrenia Am. J. Psychiatry 166 2009 226 233
79. B.I. Turetsky, P.J. Moberg, D.M. Yousem, R.L. Doty, S.E. Arnold, and R.E. Gur Reduced olfactory bulb volume in patients with schizophrenia Am. J. Psychiatry 157 2000 828 830
80. B.I. Turetsky, C.G. Hahn, S.E. Arnold, and P.J. Moberg Olfactory receptor neuron dysfunction in schizophrenia Neuropsychopharmacology 34 2009 767 774
81. B.I. Turetsky, C.G. Hahn, K. Borgmann-Winter, and P.J. Moberg Scents and nonsense: olfactory dysfunction in schizophrenia Schizophr. Bull. 35 2009 1117 1131
82. J. Vent, A.M. Robinson, M.J. Gentry-Nielsen, D.B. Conley, R. Hallworth, D.A. Leopold, and R.C. Kern Pathology of the olfactory epithelium: smoking and ethanol exposure Laryngoscope 114 2004 1383 1388
83. S. Vijayaraghavan, P.C. Pugh, Z.W. Zhang, M.M. Rathouz, and D.K. Berg Nicotinic receptors that bind alpha-bungarotoxin on neurons raise intracellular free Ca2+ Neuron 8 1992 353 362
84. N. Wanaverbecq, A. Semyanov, I. Pavlov, M.C. Walker, and D.M. Kullmann Cholinergic axons modulate GABAergic signaling among hippocampal interneurons via postsynaptic alpha 7 nicotinic receptors J. Neurosci. 27 2007 5683 5693
85. S.B. Weinberger, G.F. Koob, and J.L. Martinez Jr. Differences in one-way active avoidance learning in mice of three inbred strains Behav. Genet. 22 1992 177 188
86. G.B. Wetherhill, and H. Levitt Sequential estimation of points on a psychometric function Br. J. Math. Stat. Psychol. 18 1965 1 10
87. P. Whiteaker, A.R. Davies, M.J. Marks, I.S. Blagbrough, B.V. Potter, A.J. Wolstenholme, A.C. Collins, and S. Wonnacott 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
88. D.A. Wilson Scopolamine enhances generalization between odor representations in rat olfactory cortex Learn. Mem. 8 2001 279 285
89. J. Wu, M.S. Buchsbaum, K. Moy, N. Denlea, P. Kesslak, H. Tseng, D. Plosnaj, M. Hetu, S. Potkin, and S. Bracha Olfactory memory in unmedicated schizophrenics Schizophr. Res. 9 1993 41 47