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Science 11 March 1983:
Vol. 219. no. 4589, pp. 1184 - 1190
DOI: 10.1126/science.6338589

Articles

Science, Vol 219, Issue 4589, 1184-1190
Copyright © 1983 by American Association for the Advancement of Science


articles

Alzheimer's disease: a disorder of cortical cholinergic innervation

JT Coyle, DL Price, and MR DeLong

Great emphasis is being placed on identification of neurotransmitter systems involved in the symptomatic manifestations of neurological and psychiatric disorders. In the case of Alzheimer's disease, which now seems to be one of the most common causes of mental deterioration in the elderly, compelling evidence has been developed that acetylcholine-releasing neurons, whose cell bodies lie in the basal forebrain, selectively degenerate. These cholinergic neurons provide widespread innervation of the cerebral cortex and related structures and appear to play an important role in cognitive functions, especially memory. These advances reflect a close interaction between experimental and clinical neuroscientists in which information derived from basic neurobiology is rapidly utilized to analyze disorders of the human brain.


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References.
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J. A. H. R. Claassen and R. W. M. M. Jansen (2006)
J. Gerontol. A Biol. Sci. Med. Sci. 61, 267-271
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From The Cover: Low acetylcholine during slow-wave sleep is critical for declarative memory consolidation.
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Activation of Muscarinic Receptors Inhibits beta -Amyloid Peptide-induced Signaling in Cortical Slices.
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Muscarinic Potentiation of GABAA Receptor Currents Is Gated by Insulin Signaling in the Prefrontal Cortex.
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Two different inward rectifier K+ channels are effectors for transmitter-induced slow excitation in brain neurons.
D. Bajic, M. Koike, A. M. Albsoul-Younes, S. Nakajima, and Y. Nakajima (2002)
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Noninvasive in vivo assessment of cholinergic cortical circuits in AD using transcranial magnetic stimulation.
V. Di Lazzaro, A. Oliviero, P. A. Tonali, C. Marra, A. Daniele, P. Profice, E. Saturno, F. Pilato, C. Masullo, and J. C. Rothwell (2002)
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M. D. Santos, M. Alkondon, E. F. R. Pereira, Y. Aracava, H. M. Eisenberg, A. Maelicke, and E. X. Albuquerque (2002)
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Cholinergic Changes in the APP23 Transgenic Mouse Model of Cerebral Amyloidosis.
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Attenuation of Scopolamine-Induced and Age-Associated Memory Impairments by the Sigma and 5-Hydroxytryptamine1A Receptor Agonist OPC-14523 (1-{3-[4-(3-chlorophenyl)-1-piperazinyl]propyl}-5-methoxy-3,4-dihydro-2[1H]-quinolinone monomethanesulfonate).
K. Tottori, M. Nakai, Y. Uwahodo, T. Miwa, S. Yamada, Y. Oshiro, T. Kikuchi, and C. A. Altar (2002)
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Complete Deletion of the Neurotrophin Receptor p75NTR Leads to Long-Lasting Increases in the Number of Basal Forebrain Cholinergic Neurons.
T. Naumann, E. Casademunt, E. Hollerbach, J. Hofmann, G. Dechant, M. Frotscher, and Y.-A. Barde (2002)
J. Neurosci. 22, 2409-2418
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Neuronal nicotinic acetylcholine receptors: involvement in Alzheimer's disease and schizophrenia..
D. S. Woodruff-Pak and T. J. Gould (2002)
Behav Cogn Neurosci Rev 1, 5-20
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Aging Causes a Preferential Loss of Cholinergic Innervation of Characterized Neocortical Pyramidal Neurons.
M. A. Casu, T. Pan Wong, Y. De Koninck, A. Ribeiro-da-Silva, and A. C. Cuello (2002)
Cereb Cortex 12, 329-337
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Characterization of Central Inhibitory Muscarinic Autoreceptors by the Use of Muscarinic Acetylcholine Receptor Knock-Out Mice.
W. Zhang, A. S. Basile, J. Gomeza, L. A. Volpicelli, A. I. Levey, and J. Wess (2002)
J. Neurosci. 22, 1709-1717
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Memory loss in old rats is associated with brain mitochondrial decay and RNA/DNA oxidation: Partial reversal by feeding acetyl-L-carnitine and/or R-alpha -lipoic acid.
J. Liu, E. Head, A. M. Gharib, W. Yuan, R. T. Ingersoll, T. M. Hagen, C. W. Cotman, and B. N. Ames (2002)
PNAS 99, 2356-2361
   Abstract »    Full Text »    PDF »
Scopolamine Enhances Generalization between Odor Representations in Rat Olfactory Cortex.
D. A. Wilson (2001)
Learn. Mem. 8, 279-285
   Abstract »    Full Text »    PDF »
Hyperactivity and Intact Hippocampus-Dependent Learning in Mice Lacking the M1 Muscarinic Acetylcholine Receptor.
T. Miyakawa, M. Yamada, A. Duttaroy, and J. Wess (2001)
J. Neurosci. 21, 5239-5250
   Abstract »    Full Text »    PDF »
Behavior and treatment in frontotemporal dementia.
R. J. Perry and B. L. Miller (2001)
Neurology 56, S46-51
   Abstract »    Full Text »    PDF »
Cholinergic Modulation of Excitatory Synaptic Transmission in the CA3 Area of the Hippocampus.
K. E. Vogt and W. G. Regehr (2001)
J. Neurosci. 21, 75-83
   Abstract »    Full Text »    PDF »
Muscarinic Cholinergic Modulation of Prepulse Inhibition of the Acoustic Startle Reflex.
C. K. Jones and H. E. Shannon (2000)
J. Pharmacol. Exp. Ther. 294, 1017-1023
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Galantamine in AD: A 6-month randomized, placebo-controlled trial with a 6-month extension.
M. A. Raskind, E. R. Peskind, T. Wessel, and W. Yuan (2000)
Neurology 54, 2261-2268
   Abstract »    Full Text »    PDF »
Further Evidence for a Dissociation Between Different Forms of Mnemonic Expressions in a Mouse Model of Age-related Cognitive Decline: Effects of Tacrine and S 17092, a Novel Prolyl Endopeptidase Inhibitor.
A. Marighetto, K. Touzani, N. Etchamendy, C. C. Torrea, G. De Nanteuil, D. Guez, R. Jaffard, and P. Morain (2000)
Learn. Mem. 7, 159-169
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Nerve Growth Factor (NGF) Augments Cortical and Hippocampal Cholinergic Functioning after p75NGF Receptor-Mediated Deafferentation But Impairs Inhibitory Avoidance and Induces Fear-Related Behaviors.
J. Winkler, G. A. Ramirez, L. J. Thal, and J. J. Waite (2000)
J. Neurosci. 20, 834-844
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Cognitive changes and modified processing of amyloid precursor protein in the cortical and hippocampal system after cholinergic synapse loss and muscarinic receptor activation.
L. Lin, B. Georgievska, A. Mattsson, and O. Isacson (1999)
PNAS 96, 12108-12113
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Age-associated neuronal atrophy occurs in the primate brain and is reversible by growth factor gene therapy.
D. E. Smith, J. Roberts, F. H. Gage, and M. H. Tuszynski (1999)
PNAS 96, 10893-10898
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Basal forebrain amnesia: does the nucleus accumbens contribute to human memory?.
G. Goldenberg, U. Schuri, O. Gromminger, and U. Arnold (1999)
J. Neurol. Neurosurg. Psychiatry 67, 163-168
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Improved Cognition in Alzheimer's Disease With Short-Term D-Cycloserine Treatment.
G. E. Tsai, W. E. Falk, J. Gunther, and J. T. Coyle (1999)
Am J Psychiatry 156, 467-469
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In vivo mapping of cerebral acetylcholinesterase activity in aging and Alzheimer's disease.
D. E. Kuhl, R. A. Koeppe, S. Minoshima, S. E. Snyder, E. P. Ficaro, N. L. Foster, K. A. Frey, and M. R. Kilbourn (1999)
Neurology 52, 691
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Improving Effects of Huperzine A on Spatial Working Memory in Aged Monkeys and Young Adult Monkeys with Experimental Cognitive Impairment.
J. W. Ye, J. X. Cai, L. M. Wang, and X. C. Tang (1999)
J. Pharmacol. Exp. Ther. 288, 814-819
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ONO-1603, a Potential Antidementia Drug, Delays Age-Induced Apoptosis and Suppresses Overexpression of Glyceraldehyde-3-Phosphate Dehydrogenase in Cultured Central Nervous System Neurons.
N. Katsube, K. Sunaga, H. Aishita, D.-M. Chuang, and R. Ishitani (1999)
J. Pharmacol. Exp. Ther. 288, 6-13
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Dexamethasone Induces Hypertrophy of Developing Medial Septum Cholinergic Neurons: Potential Role of Nerve Growth Factor.
B. Shi, S. J. Rabin, C. Brandoli, and I. Mocchetti (1998)
J. Neurosci. 18, 9326-9334
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beta -Adrenergic receptor-induced activation of nerve growth factor gene transcription in rat cerebral cortex involves CCAAT/enhancer-binding protein delta.
A. M. Colangelo, P. F. Johnson, and I. Mocchetti (1998)
PNAS 95, 10920-10925
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Cholinergic Switching Within Neocortical Inhibitory Networks.
Z. Xiang, J. R. Huguenard, and D. A. Prince (1998)
Science 281, 985-988
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Increased Calcium Buffering in Basal Forebrain Neurons During Aging.
D. Murchison and W. H. Griffith (1998)
J Neurophysiol 80, 350-364
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Estrogen Therapy in Postmenopausal Women: Effects on Cognitive Function and Dementia.
K. Yaffe, G. Sawaya, I. Lieberburg, and D. Grady (1998)
JAMA 279, 688-695
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Effects of U-50,488H on Scopolamine-, Mecamylamine- and Dizocilpine-Induced Learning and Memory Impairment in Rats.
M. Hiramatsu, H. Murasawa, T. Nabeshima, and T. Kameyama (1998)
J. Pharmacol. Exp. Ther. 284, 858-867
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Neurosteroids: Deficient cognitive performance in aged rats depends on low pregnenolone sulfate levels in the hippocampus.
M. Vallee, W. Mayo, M. Darnaudery, C. Corpechot, J. Young, M. Koehl, M. Le Moal, E.-E. Baulieu, P. Robel, and H. Simon (1997)
PNAS 94, 14865-14870
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Peroxide Modulation of Slow Onset Potentiation in Rat Hippocampus.
J. M. Auerbach and M. Segal (1997)
J. Neurosci. 17, 8695-8701
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Cerebral cortical astroglia from the trisomy 16 mouse, a model for Down syndrome, produce neuronal cholinergic deficits in cell culture.
P. G. Nelson, S. Fitzgerald, S. I. Rapoport, E. A. Neale, Z. Galdzicki, V. Dunlap, L. Bowers, and D. v. Agoston (1997)
PNAS 94, 12644-12648
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Life and Death of Neurons in the Aging Brain.
J. H. Morrison and P. R. Hof (1997)
Science 278, 412-419
   Abstract »    Full Text »
A Role for TrkA during Maturation of Striatal and Basal Forebrain Cholinergic Neurons In Vivo.
A. M. Fagan, M. Garber, M. Barbacid, I. Silos-Santiago, and D. M. Holtzman (1997)
J. Neurosci. 17, 7644-7654
   Abstract »    Full Text »    PDF »
ABT-089 [2-Methyl-3-(2-(S)-pyrrolidinylmethoxy)pyridine]: I. A Potent and Selective Cholinergic Channel Modulator with Neuroprotective Properties.
J. P. Sullivan, D. Donnelly-Roberts, C. A. Briggs, D. J. Anderson, M. Gopalakrishnan, I. C. Xue, M. Piattoni-Kaplan, E. Molinari, J. E. Campbell, D. G. Mckenna, et al. (1997)
J. Pharmacol. Exp. Ther. 283, 235-246
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ABT-089 [2-Methyl-3-(2-(S)-pyrrolidinylmethoxy)pyridine dihydrochloride]: II. A Novel Cholinergic Channel Modulator with Effects on Cognitive Performance in Rats and Monkeys.
M. W. Decker, A. W. Bannon, P. Curzon, K. L. Gunther, J. D. Brioni, M. W. Holladay, N.-H. Lin, Y. Li, J. F. Daanen, J. J. Buccafusco, et al. (1997)
J. Pharmacol. Exp. Ther. 283, 247-258
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Regulation of Human alpha 4beta 2 Neuronal Nicotinic Acetylcholine Receptors by Cholinergic Channel Ligands and Second Messenger Pathways.
M. Gopalakrishnan, E. J. Molinari, and J. P. Sullivan (1997)
Mol. Pharmacol. 52, 524-534
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Effects of Xanomeline, a Selective Muscarinic Receptor Agonist, on Cognitive Function and Behavioral Symptoms in Alzheimer Disease.
N. C. Bodick, W. W. Offen, A. I. Levey, N. R. Cutler, S. G. Gauthier, A. Satlin, H. E. Shannon, G. D. Tollefson, K. Rasmussen, F. P. Bymaster, et al. (1997)
Arch Neurol 54, 465-473
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FK960 [N-(4-Acetyl-1-piperazinyl)-p-fluorobenzamide Monohydrate], a Novel Potential Antidementia Drug, Improves Visual Recognition Memory in Rhesus Monkeys: Comparison with Physostigmine.
N. Matsuoka and T. G. Aigner (1997)
J. Pharmacol. Exp. Ther. 280, 1201-1209
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Neurochemical Effects of 3-[1-(Phenylmethyl)-4-Piperidinyl]-1-(2,3,4,5-Tetrahydro-1H-1-Benzazepin-8-yl)-1-Propanone Fumarate (TAK-147), a Novel Acetylcholinesterase Inhibitor, in Rats.
K. Hirai, K. Kato, T. Nakayama, H. Hayako, Y. Ishihara, G. Goto, and M. Miyamoto (1997)
J. Pharmacol. Exp. Ther. 280, 1261-1269
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Pharmacological Activity and Safety Profile of P10358, a Novel, Orally Active Acetylcholinesterase Inhibitor for Alzheimer's Disease.
C. P. Smith, G. M. Bores, W. Petko, M. Li, D. E. Selk, D. K. Rush, F. Camacho, J. T. Winslow, R. Fishkin, D. M. Cunningham, et al. (1997)
J. Pharmacol. Exp. Ther. 280, 710-720
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Modulation of Inhibitory Transmission by Dopamine in Rat Basal Forebrain Nuclei: Activation of Presynaptic D1-like Dopaminergic Receptors.
T. Momiyama and J. A. Sim (1996)
J. Neurosci. 16, 7505-7512
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Muscarinic acetylcholine receptor expression in memory circuits: Implications for treatment of Alzheimer disease.
A. I. Levey (1996)
PNAS 93, 13541-13546
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Estrogen Replacement Therapy and Risk of Alzheimer Disease.
A. Paganini-Hill and V. W. Henderson (1996)
Arch Intern Med 156, 2213-2217
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Cholinergic Changes in the Hippocampus of Stroke-Prone Spontaneously Hypertensive Rats.
H. Togashi, S. Kimura, M. Matsumoto, M. Yoshioka, M. Minami, and H. Saito (1996)
Stroke 27, 520-526
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A Signaling Endosome Hypothesis to Explain NGF Actions: Potential Implications for Neurodegeneration.
E.C. Beattie, J. Zhou, M.L. Grimes, N.W. Bunnett, C.L. Howe, and W.C. Mobley (1996)
Cold Spring Harb Symp Quant Biol 61, 389-406
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Cognitive Test Performance in Detecting, Staging, and Tracking Alzheimer's Disease.
J. J. Locascio, J. H. Growdon, and S. Corkin (1995)
Arch Neurol 52, 1087-1099
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Biologic Markers and Neurochemical Correlates of Agitation and Psychosis in Dementia.
M. Kirby and B. A. Lawlor (1995)
J Geriatr Psychiatry Neurol 8, S2-S7
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J. F. Patterson (1988)
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