Aged dogs demonstrate both increased sensitivity to scopolamine impairment and decreased muscarinic receptor density

Pharmacology Biochemistry and Behavior

Volumn 98, Issue 2, 2011, Pages 203-209

  Araujo, Joseph A ^a,b   Nobrega, José N ^a,c   Raymond, Roger ^a,c   Milgram, Norton W ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b CanCog Technologies Incorporated   (Canada)

^c CENTRE FOR ADDICTION AND MENTAL HEALTH   (Canada)

Author keywords

Alzheimers disease; Cholinergic system; Dog; Memory; Muscarinic receptors; Scopolamine

Indexed keywords

AMYLOID BETA PROTEIN; MUSCARINIC RECEPTOR; QUINUCLIDINYL BENZILATE; SCOPOLAMINE;

AGED; AGING; ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTORADIOGRAPHY; BRAIN REGION; CEREBELLUM; CHOLINERGIC SYSTEM; COGNITIVE DEFECT; CONTROLLED STUDY; DOG; FEMALE; FUNCTIONAL ASSESSMENT; MALE; NONHUMAN; PRIORITY JOURNAL; RECEPTOR BINDING; RECEPTOR DENSITY; SPATIAL MEMORY; TASK PERFORMANCE;

AGING; ALZHEIMER DISEASE; ANIMALS; BRAIN; DOGS; FEMALE; HUMANS; MALE; MEMORY, SHORT-TERM; MODELS, ANIMAL; MUSCARINIC ANTAGONISTS; RECEPTORS, MUSCARINIC; SCOPOLAMINE; TISSUE DISTRIBUTION;

CANIS FAMILIARIS;

EID: 78951488644     PISSN: 00913057     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbb.2011.01.005     Document Type: Article

References (73)

1. B. Adams, A. Chan, H. Callahan, and N.W. Milgram The canine as a model of human cognitive aging: recent developments Prog Neuropsychopharmacol Biol Psychiatry 24 2000 675 692 (Pubitemid 30640154)
2. B. Adams, A. Chan, H. Callahan, C. Siwak, D. Tapp, and C. Ikeda-Douglas Use of a delayed non-matching to position task to model age-dependent cognitive decline in the dog Behav Brain Res 108 2000 47 56 (Pubitemid 30009726)
3. J.A. Araujo, A.D. Chan, L.L. Winka, P.A. Seymour, and N.W. Milgram Dose-specific effects of scopolamine on canine cognition: impairment of visuospatial memory, but not visuospatial discrimination Psychopharmacology 175 2004 92 98 (Pubitemid 39215535)
4. R.T. Bartus On neurodegenerative diseases, models, and treatment strategies: lessons learned and lessons forgotten a generation following the cholinergic hypothesis Exp Neurol 163 2000 495 529 (Pubitemid 30399100)
5. R.T. Bartus, R.L. Dean III, B. Beer, and A.S. Lippa The cholinergic hypothesis of geriatric memory dysfunction Science 217 1982 408 414
6. S.L. Biggan, J.L. Ingles, and R.J. Beninger Scopolamine differentially affects memory of 8- and 16-month-old rats in the double Y-maze Neurobiol Aging 17 1996 25 30
7. J. Birks Cholinesterase inhibitors for Alzheimers disease Cochrane Database Syst Rev 2006 CD005593
8. P. Broks, G.C. Preston, M. Traub, P. Poppleton, C. Ward, and S.M. Stahl Modelling dementia: effects of scopolamine on memory and attention Neuropsychol 26 1988 685 700
9. H. Callahan, C. Ikeda-Douglas, E. Head, C.W. Cotman, and N.W. Milgram Development of a protocol for studying object recognition memory in the dog Prog Neuropsychopharmacol Biol Psychiatry 24 2000 693 707 (Pubitemid 30640155)
10. A.D. Chan, P.M. Nippak, H. Murphey, C.J. Ikeda-Douglas, B. Muggenburg, and E. Head Visuospatial impairments in aged canines (Canis familiaris): the role of cognitive-behavioral flexibility Behav Neurosci 116 2002 443 454 (Pubitemid 34533580)
11. M.L. Cheal Scopolamine disrupts maintenance of attention rather than memory processes Behav Neural Biol 33 1981 163 187 (Pubitemid 12217677)
12. K.C. Chen, M.G. Baxter, and J.S. Rodefer Central blockade of muscarinic cholinergic receptors disrupts affective and attentional set-shifting Eur J Neurosci 20 2004 1081 1088 (Pubitemid 39141315)
13. A. Contestabile, E. Ciani, and A. Contestabile The place of choline acetyltransferase activity measurement in the "cholinergic hypothesis" of neurodegenerative diseases Neurochem Res 33 2008 318 327
14. C.W. Cotman, and E. Head The canine (dog) model of human aging and disease: dietary, environmental and immunotherapy approaches J Alzheimers Dis 15 2008 685 707
15. B.J. Cummings, E. Head, W. Ruehl, N.W. Milgram, and C.W. Cotman The canine as an animal model of human aging and dementia Neurobiol Aging 17 1996 259 268 (Pubitemid 26167637)
16. M.C. Davidson, E.B. Cutrell, and R.T. Marrocco Scopolamine slows the orienting of attention in primates to cued visual targets Psychopharmacology 142 1999 1 8 (Pubitemid 29196057)
17. P. Davies, and A.J. Maloney Selective loss of central cholinergic neurons in Alzheimers disease Lancet 2 1976 1403 (Pubitemid 8004505)
18. M.W. Decker The effects of aging on hippocampal and cortical projections of the forebrain cholinergic system Brain Res 434 1987 423 438 (Pubitemid 17152529)
19. M.W. Decker, and J.L. McGaugh The role of interactions between the cholinergic system and other neuromodulatory systems in learning and memory Synapse 7 1991 151 168
20. R.S. Doody Current treatments for Alzheimers disease: cholinesterase inhibitors J Clin Psychiatry 64 Suppl-7 2003
21. D.A. Drachman, and J. Leavitt Human memory and the cholinergic system. A relationship to aging? Arch Neurol 30 1974 113 121
22. M.P. Dunne, and L.R. Hartley Scopolamine and the control of attention in humans Psychopharmacology 89 1986 94 97 (Pubitemid 16062970)
23. H.C. Fibiger, G. Damsma, and J.C. Day Behavioral pharmacology and biochemistry of central cholinergic neurotransmission Adv Exp Med Biol 295 1991 399 414
24. A. Fisher M1 muscarinic agonists target major hallmarks of Alzheimers disease - the pivitol role of brain M1 receptors. Neurodegener Dis 5 2008 237 240 (Pubitemid 351347860)
25. C. Flicker, S.H. Ferris, and M. Serby Hypersensitivity to scopolamine in the elderly Psychopharmacology 107 1992 437 441
26. M.L. Furey, P. Pietrini, J.V. Haxby, and W.C. Drevets Selective effects of cholinergic modulation on task performance during selective attention Neuropsychopharmacol 33 2008 913 923 (Pubitemid 351252696)
27. M. Gallagher, and P.J. Colombo Ageing: the cholinergic hypothesis of cognitive decline Curr Opin Neurobiol 5 1995 161 168
28. M. Hamann, R. Raymond, S. Varughesi, J.N. Nobrega, and A. Richter Acetylcholine receptor binding and cholinergic interneuron density are unaltered in a genetic animal model of primary paroxysmal dystonia Brain Res 1099 2006 176 182 (Pubitemid 44080093)
29. J.A. Hardy, and G.A. Higgins Alzheimers disease: the amyloid cascade hypothesis Science 256 1992 184 185
30. E. Head, H. Callahan, B.A. Muggenburg, C.W. Cotman, and N.W. Milgram Visual-discrimination learning ability and beta-amyloid accumulation in the dog Neurobiol Aging 19 1998 415 425 (Pubitemid 29065491)
31. E. Head, R. McCleary, F.F. Hahn, N.W. Milgram, and C.W. Cotman Region-specific age at onset of beta-amyloid in dogs Neurobiol Aging 21 2000 89 96 (Pubitemid 30224790)
32. E. Head, R. Mehta, J. Hartley, M. Kameka, B.J. Cummings, and C.W. Cotman Spatial learning and memory as a function of age in the dog Behav Neurosci 109 1995 851 858
33. E. Hellstrom-Lindahl Modulation of beta-amyloid precursor protein processing and tau phosphorylation by acetylcholine receptors Eur J Pharmacol 393 2000 255 263 (Pubitemid 30193425)
34. F.J. Huff, S.F. Mickel, S. Corkin, and J.H. Growdon Cognitive functions affected by scopolamine in Alzheimers disease and normal aging Drug Dev Res 12 1988 271 278
35. R. Jakob-Roetne, and H. Jacobsen Alzheimers disease: from pathology to therapeutic approaches Angew Chem Int 48 2009 3030 3059
36. D.N. Jones, and G.A. Higgins Effect of scopolamine on visual attention in rats Psychopharmacol 120 1995 142 149
37. O. Lehmann, A.J. Grottick, J.C. Cassel, and G.A. Higgins A double dissociation between serial reaction time and radial maze performance in rats subjected to 192 IgG-saporin lesions of the nucleus basalis and/or the septal region. Eur J Neurosci 18 2003 651 666 (Pubitemid 37041113)
38. A.L. Markowska, D.S. Olton, and B. Givens Cholinergic manipulations in the medial septal area: age-related effects on working memory and hippocampal electrophysiology J Neurosci 15 1995 2063 2073
39. J. McGaughy, B.J. Everitt, T.W. Robbins, and M. Sarter The role of cortical cholinergic afferent projections in cognition: impact of new selective immunotoxins Behav Brain Res 115 2000 251 263
40. J. McGaughy, J. Turchi, and M. Sarter Crossmodal divided attention in rats: effects of chlordiazepoxide and scopolamine Psychopharmacology 115 1994 213 220 (Pubitemid 24207784)
41. P.L. McGeer, E.G. McGeer, J. Suzuki, C.E. Dolman, and T. Nagai Aging, Alzheimers disease, and the cholinergic system of the basal forebrain Neurol 34 1984 741 745 (Pubitemid 14107071)
42. N.W. Milgram Cognitive experience and its effect on age-dependent cognitive decline in beagle dogs Neurochem Res 28 2003 1677 1682 (Pubitemid 37296209)
43. N.W. Milgram, E. Head, B. Muggenburg, D. Holowachuk, H. Murphey, and J. Estrada Landmark discrimination learning in the dog: effects of age, an antioxidant fortified food, and cognitive strategy Neurosci Biobehav Rev 26 2002 679 695 (Pubitemid 36002018)
44. N.W. Milgram, E. Head, E. Weiner, and E. Thomas Cognitive functions and aging in the dog: acquisition of nonspatial visual tasks Behav Neurosci 108 1994 57 68 (Pubitemid 24097744)
45. N.W. Milgram, C.T. Siwak-Tapp, J. Araujo, and E. Head Neuroprotective effects of cognitive enrichment Ageing Res Rev 5 2006 354 369 (Pubitemid 44374431)
46. N.W. Milgram, S.C. Zicker, E. Head, B.A. Muggenburg, H. Murphey, and C.J. Ikeda-Douglas Dietary enrichment counteracts age-associated cognitive dysfunction in canines Neurobiol Aging 23 2002 737 745 (Pubitemid 35217699)
47. H. Moore, P. Dudchenko, K.S. Comer, J.P. Bruno, and M. Sarter Central versus peripheral effects of muscarinic antagonists: the limitations of quaternary ammonium derivatives Psychopharmacology 108 1992 241 243
48. J.L. Muir Acetylcholine, aging, and Alzheimers disease Pharmacol Biochem Behav 56 1997 687 696
49. L. Nobili, and W.G. Sannita Cholinergic modulation, visual function and Alzheimers dementia Vis Res 37 1997 3559 3571 (Pubitemid 27491635)
50. R. Norbury, M.J. Travis, K. Erlandsson, W. Waddington, J. Owens, and S. Pimlott In vivo imaging of muscarinic receptors in the aging female brain with (R, R)[123I]-I-QNB and single photon emission tomography Exp Gerontol 40 2005 137 145 (Pubitemid 40343004)
51. M. Pakaski, and J. Kalman Interactions between the amyloid and cholinergic mechanisms in Alzheimers disease Neurochem Int 53 2008 103 111
52. N. Papaioannou, P.C. Tooten, A.M. van Ederen, J.R. Bohl, J. Rofina, and T. Tsangaris Immunohistochemical investigation of the brain of aged dogs. I. Detection of neurofibrillary tangles and of 4-hydroxynonenal protein, an oxidative damage product, in senile plaques Amyloid 8 2001 11 21 (Pubitemid 32210176)
53. G. Pepeu, and M.G. Giovannini Cholinesterase inhibitors and beyond Curr Alzheimer Res 6 2009 86 96
54. E.K. Perry, P.H. Gibson, G. Blessed, R.H. Perry, and B.E. Tomlinson Neurotransmitter enzyme abnormalities in senile dementia. Choline acetyltransferase and glutamic acid decarboxylase activities in necropsy brain tissue J Neurol Sci 34 1977 247 265 (Pubitemid 8188071)
55. E.K. Perry, B.E. Tomlinson, G. Blessed, K. Bergmann, P.H. Gibson, and R.H. Perry Correlation of cholinergic abnormalities with senile plaques and mental test scores in senile dementia Br Med J 2 1978 1457 1459 (Pubitemid 9061468)
56. E. Portelius, N. Bogdanovic, M.K. Gustavsson, I. Volkmann, G. Brinkmalm, and H. Zetterberg Mass spectrometric characterization of brain amyloid beta isoform signatures in familial and sporadic Alzheimers disease Acta Neuropathol 120 2010 185 193
57. M. Pugliese, J. Mascort, N. Mahy, and I. Ferrer Diffuse beta-amyloid plaques and hyperphosphorylated tau are unrelated processes in aged dogs with behavioral deficits Acta Neuropath 112 2006 175 183
58. P.G. Ray, K.J. Meador, D.W. Loring, E.W. Zamrini, X.H. Yang, and J.J. Buccafusco Central anticholinergic hypersensitivity in aging J Ger Psychiatry Neurol 5 1992 72 77
59. K.J. Reinikainen, P.J. Riekkinen, T. Halonen, and M. Laakso Decreased muscarinic receptor binding in cerebral cortex and hippocampus in Alzheimers disease Life Sci 41 1987 453 461 (Pubitemid 17105224)
60. U.D. Renner, R. Oertel, and W. Kirch Pharmacokinetics and pharmacodynamics in clinical use of scopolamine Ther Drug Monit 27 2005 655 665 (Pubitemid 41439741)
61. J.O. Rinne, K. Laakso, P. Lonnberg, P. Molsa, L. Paljarvi, and J.K. Rinne Brain muscarinic receptors in senile dementia Brain Res 336 1985 19 25 (Pubitemid 15013857)
62. R. Rodriguez-Puertas, J. Pascual, T. Vilaro, and A. Pazos Autoradiographic distribution of M1, M2, M3, and M4 muscarinic receptor subtypes in Alzheimers disease Synapse 26 1997 341 350 (Pubitemid 27284105)
63. J. Stemmelin, J.C. Cassel, B. Will, and C. Kelche Sensitivity to cholinergic drug treatments of aged rats with variable degrees of spatial memory impairment Behav Brain Res 98 1999 53 66 (Pubitemid 28566196)
64. C.M. Studzinski, L.A. Christie, J.A. Araujo, W.M. Burnham, E. Head, and C.W. Cotman Visuospatial function in the beagle dog: an early marker of cognitive decline in a model of human aging and dementia Neurobiol Learn Mem 86 2006 197 204 (Pubitemid 44287579)
65. M.Y. Su, E. Head, W.M. Brooks, Z. Wang, B.A. Muggenburg, and G.E. Adam Magnetic resonance imaging of anatomic and vascular characteristics in a canine model of human aging Neurobiol Aging 19 1998 479 485 (Pubitemid 29065497)
66. T. Sunderland, P.N. Tariot, R.M. Cohen, H. Weingartner, E.A. Mueller III, and D.L. Murphy Anticholinergic sensitivity in patients with dementia of the Alzheimer type and age-matched controls. A dose-response study Arch Gen Psychiatry 44 1987 418 426 (Pubitemid 17064486)
67. P.D. Tapp, C.T. Siwak, J. Estrada, E. Head, B.A. Muggenburg, and C.W. Cotman Size and reversal learning in the beagle dog as a measure of executive function and inhibitory control in aging Learn Mem 10 2003 64 73 (Pubitemid 36177022)
68. P.D. Tapp, C.T. Siwak, J. Estrada, D. Holowachuk, and N.W. Milgram Effects of age on measures of complex working memory span in the beagle dog (Canis familiaris) using two versions of a spatial list learning paradigm Learn Mem 10 2003 148 160 (Pubitemid 36418725)
69. P.D. Tapp, C.T. Siwak, F.Q. Gao, J.Y. Chiou, S.E. Black, and E. Head Frontal lobe volume, function, and beta-amyloid pathology in a canine model of aging J Neurosci 24 2004 8205 8213 (Pubitemid 39280799)
70. J. Wegiel, H.M. Wisniewski, and Z. Soltysiak Region- and cell-type-specific pattern of tau phosphorylation in dog brain Brain Res 802 1998 259 266 (Pubitemid 28392179)
71. P.J. Whitehouse, D.L. Price, A.W. Clark, J.T. Coyle, and M.R. DeLong Alzheimer disease: evidence for selective loss of cholinergic neurons in the nucleus basalis Ann Neurol 10 1981 122 126 (Pubitemid 11053099)
72. D.S. Woodruff-Pak Animal models of Alzheimers disease: therapeutic implications J Alzheimers Dis 15 2008 507 521
73. J.K. Zubieta, R.A. Koeppe, K.A. Frey, M.R. Kilbourn, T.J. Mangner, and N.L. Foster Assessment of muscarinic receptor concentrations in aging and Alzheimer disease with [11 C]NMPB and PET Synapse 39 2001 275 287 (Pubitemid 32128649)