Selective cognitive dysfunction in acetylcholine M1 muscarinic receptor mutant mice

Nature Neuroscience

Volumn 6, Issue 1, 2003, Pages 51-58

  Anagnostaras, Stephan G ^a,b   Murphy, Geoffrey G ^a   Hamilton, Susan E ^c   Mitchell, Scott L ^a,b   Rahnama, Nancy P ^a   Nathanson, Neil M ^c   Silva, Alcino J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b EMORY UNIVERSITY   (United States)

^c UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MUSCARINIC M1 RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHOLINERGIC SYSTEM; CONDITIONING; CONTROLLED STUDY; FEAR; HIPPOCAMPUS; LONG TERM POTENTIATION; MAZE TEST; MEMORY CONSOLIDATION; MEMORY DISORDER; MOUSE; NONHUMAN; PRIORITY JOURNAL; WORKING MEMORY;

ACETYLCHOLINE; ANIMALS; CEREBRAL CORTEX; CONDITIONING (PSYCHOLOGY); CUES; DISCRIMINATION LEARNING; ELECTRIC STIMULATION; FEAR; FEMALE; HIPPOCAMPUS; MALE; MAZE LEARNING; MEMORY; MEMORY DISORDERS; MEMORY, SHORT-TERM; MICE; MICE, KNOCKOUT; MUTATION; NEURAL PATHWAYS; PHENOTYPE; RECEPTOR, MUSCARINIC M1; RECEPTORS, MUSCARINIC;

EID: 0037220723     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn992     Document Type: Article

References (50)

1. Caulfield, M.P. & Birdsall, N.J. Classification of muscarinic acetylcholine receptors. Pharmacol. Rev. 50, 279-290 (1998).
2. Fornari, R.V., Moreira, K.M. & Oliveira, M.G. Effects of the selective M1 muscarinic receptor antagonist dicyclomine on emotional memory. Learn. Mem. 7, 287-292 (2000).
3. Wallis, R.M. & Napier, C.M. Muscarinic antagonists in development for disorders of smooth muscle function. Life Sci. 64, 395-401 (1999).
4. Levey, A.I., Kitt, C.A., Simonds, W.F., Price, D.L. & Brann, M.R. Identification and localization of muscarinic acetylcholine receptor proteins in brain with subtype-specific antibodies. J. Neurosci. 11, 3218-3226 (1991).
5. Wei, J., Walton, E.A., Milici, A. & Buccafusco, J.J. m1-m5 muscarinic receptor distribution in rat CNS by RT-PCR and HPLC. J. Neurochem. 63, 815-821 (1994).
6. Marino, M.J., Rouse, S.T., Levey, A.I., Potter, L.T. & Conn, P.J. Activation of the genetically defined m1 muscarinic receptor potentiates N-methyl-D-aspartate (NMDA) receptor currents in hippocampal pyramidal cells. Proc. Natl. Acad. Sci. USA 95, 11465-11470 (1998).
7. Hamilton, S.E. & Nathanson, N.M. The M1 receptor is required for muscarinic activation of mitogen-activated protein (MAP) kinase in murine cerebral cortical neurons. J. Biol. Chem. 276, 15850-15853 (2001).
8. Hamilton, S.E. et al. Disruption of the m1 receptor gene ablates muscarinic receptor-dependent M current regulation and seizure activity in mice. Proc. Natl. Acad. Sci. USA 94, 13311-13316 (1997).
9. Anagnostaras, S.G., Maren, S., Sage, J.R., Goodrich, S. & Fanselow, M.S. Scopolamine and Pavlovian fear conditioning in rats: Dose-effect analysis. Neuropsychopharmacology 21, 731-744 (1999).
10. Anagnostaras, S.G., Maren, S. & Fanselow, M.S. Temporally graded retrograde amnesia of contextual fear after hippocampal damage in rats: Within-subjects examination. J. Neurosci. 19, 1106-1114 (1999).
11. Levy, A., Kluge, P.B. & Elsmore, T.F. Radial arm maze performance of mice: Acquisition and atropine effects. Behav. Neural Biol. 39, 229-240 (1983).
12. Olton, D., Becker, J. & Handelmann, G. Hippocampus, space and memory. Behav. Brain Sci. 2, 313-365 (1979).
13. Hagen, J.J., Tweedie, F. & Morris, R.G.M. Lack of task specificy and absence of post-training effects of atropine on learning. Behav. Neurosci. 100, 483-493 (1986).
14. Morris, R.G.M., Garrud, P., Rawlins, J.N.P. & O'Keefe, J. Place navigation impaired in rats with hippocampal lesions. Nature 297, 681-683 (1982).
15. Winslow, J.T. & Camacho, F. Cholinergic modulation of a decrement in social investigation following repeated contacts between mice. Psychopharmacology (Berl.) 121, 164-172 (1995).
16. Kogan, J.H., Frankland, P.W. & Silva, A.J. Long-term memory underlying hippocampus-dependent social recognition in mice. Hippocampus 10, 47-56 (2000).
17. Huerta, P.T. & Lisman, J.E. Bidirectional synaptic plasticity induced by a single burst during cholinergic theta oscillation in CA1 in vitro. Neuron 15, 1053-1063 (1995).
18. Kim, J.J. & Fanselow, M.S. Modality-specific retrograde amnesia of fear. Science 256, 675-677 (1992).
19. Phillips, R.G. & LeDoux, J.E. Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav. Neurosci. 106, 274-285 (1992).
20. Rudy, J.W. Scopolamine administered before and after training impairs both contextual and auditory-cue fear conditioning. Neurobiol. Learn. Mem. 65, 73-81 (1996).
21. Gale, G.D., Anagnostaras, S.G. & Fanselow, M.S. Cholinergic modulation of Pavlovian fear conditioning: Effects of intra-hippocampal scopolamine infusion. Hippocampus 11, 371-376 (2001).
22. Wallenstein, G.V. & Vago, D.R. Intrahippocampal scopolamine impairs both acquisition and consolidation of contextual fear conditioning. Neurobiol. Learn. Mem. 75, 245-252 (2001).
23. Anagnostaras, S.G., Josselyn, S.A., Frankland, P.W. & Silva, A.J. Computer-assisted behavioral assessment of Pavlovian fear conditioning in mice. Learn. Mem. 7, 58-72 (2000).
24. Maren, S., Anagnostaras, S.G. & Fanselow, M.S. The startled seahorse: Is the hippocampus necessary for contextual fear conditioning? Trends Cogn. Sci. 2, 39-42 (1998).
25. Frankland, P.W., O'Brien, C., Ohno, M., Kirkwood, A. & Silva, A.J. Alpha-CaMKII-dependent plasticity in the cortex is required for permanent memory. Nature 411, 309-313 (2001).
26. Anagnostaras, S.G., Gale, G.D. & Fanselow, M.S. Hippocampus and contextual fear conditioning: Recent controversies and advances. Hippocarnpus 11, 8-17 (2001).
27. Phillips, R.G. & LeDoux, J.E. Lesions of the dorsal hippocampal formation interfere with background but not foreground contextual fear conditioning. Learn. Mem. 1, 34-44 (1994).
28. Frankland, P.W., Cestari, V., Filipkowski, R.K., McDonald, R.J. & Silva, A.J. The dorsal hippocampus is essential for context discrimination but not for contextual conditioning. Behav. Neurosci. 112, 863-874 (1998).
29. Maren, S., Aharonov, G. & Fanselow, M.S. Neurotoxic lesions of the dorsal hippocampus and Pavlovian fear conditioning in rats. Behav. Brain Res. 88, 261-274 (1997).
30. Bontempi, B., Laurent-Demir, C., Destrade, C. & Jaffard, R. Time-dependent reorganization of brain circuitry underlying long-term memory storage. Nature 400, 671-675 (1999).
31. Cain, D.P. Testing the NMDA, long-term potentiation, and cholinergic hypotheses of spatial learning. Neurosci. Biobehav. Rev. 22, 181-193 (1998).
32. Gerber, D.J. et al. Hyperactivity, elevated dopaminergic transmission, and response to amphetamine in M1 muscarinic acetylcholine receptor-deficient mice. Proc. Natl. Acad. Sci. USA 98, 15312-15317 (2001).
33. Miyakawa, T., Yamada, M., Duttaroy, A. & Wess, J. Hyperactivity and intact hippocampus-dependent learning in mice lacking the M1 muscarinic acetylcholine receptor. J. Neurosci. 21, 5239-5250 (2001).
34. Squire, L.R. Memory and the hippocampus: A synthesis from findings with rat, monkeys, and humans. Psychol. Rev. 99, 195-231 (1992).
35. Silva, A.J., Paylor, R., Wehner, J.M. & Tonegawa, S. Impaired spatial learning in alpha-calcium-calmodulin kinase II mutant mice. Science 257, 206-211 (1992).
36. Mayford, M. et al. Control of memory formation through regulated expression of a CaMKII transgene. Science 274, 1678-1683 (1996).
37. Bourtchuladze, R. et al. Deficient long-term memory in mice with a targeted mutation of the cAMP-responsive element-binding protein. Cell 79, 59-68 (1994).
38. Hamilton, S.E. et al. Alteration of cardiovascular and neuronal function in M1 knockout mice. Life Sci. 68, 2489-2493 (2001).
39. Eichenbaum, H., Otto, T. & Cohen, N. Two functional components of the hippocampal memory system. Behav. Brain Sci. 17, 449-518 (1994).
40. Olton, D.S. Discrimination reversal performance after hippocampal lesions: An enduring failure of reinforcement and non-reinforcement to direct behavior. Physiol. Behav. 9, 353-356 (1972).
41. Konorski, J. Integrative Activity of the Brain (Univ. of Chicago Press, Chicago, Illinois, 1967).
42. Fransen, E., Alonso, A.A. & Hasselmo, M.E. Simulations of the role of the muscarinic-activated calcium-sensitive nonspecific cation current INCM in entorhinal neuronal activity during delayed matching tasks. J. Neurosci. 22, 1081-1097 (2002).
43. Dias, R. & Aggleton, J.P. Effects of selective excitotoxic prefrontal lesions on acquisition of nonmatching and matching-to-place in the T-maze in the rat: Differential involvement of the prelimbic-infralimbic and anterior cingulate cortices in providing behavioural flexibility. Eur. J. Neurosci. 12, 4457-4466 (2000).
44. D'Esposito, M. & Postle, B.R. The dependence of span and delayed-response performance on prefrontal cortex. Neuropsychologia 37, 1303-1315 (1999).
45. Hasselmo, M. Neuromodulation: Acetylcholine and memory modulation. Trends Cogn. Sci. 3, 351-359 (1999).
46. Buzsaki, G. Two-stage model of memory trace formation: A role for "noisy" brain states. Neuroscience 31, 551-570 (1989).
47. Alreja, M. et al. Muscarinic tone sustains impulse flow in the septohippocampal GABA but not cholinergic pathway: Implications for learning and memory. J. Neurosci. 20, 8103-8110 (2000).
48. Shiozaki, K., Iseki, E., Hino, H. & Kosaka, K. Distribution of m1 muscarinic acetylcholine receptors in the hippocampus of patients with Alzheimer's disease and dementia with Lewy bodies-an immunohistochemical study. J. Neurol. Sci. 193, 23-28 (2001).
49. Levey, A.I., Edmunds, S.M., Koliatsos, V., Wiley, R.G. & Heilman, C.J. Expression of m1-m4 muscarinic acetylcholine receptor proteins in rat hippocampus and regulation by cholinergic innervation. J. Neurosci. 15, 4077-4092 (1995).
50. Bussiere, T. et al. Stereologic assessment of the total cortical volume occupied by amyloid deposits and its relationship with cognitive status in aging and Alzheimer's disease. Neuroscience 112, 75-91 (2002).