Patterns of brain acetylcholine release predict individual differences in preferred learning strategies in rats

Neurobiology of Learning and Memory

Volumn 79, Issue 2, 2003, Pages 177-183

  McIntyre, Christa K ^a   Marriott, Lisa K ^b   Gold, Paul E ^c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Acetylcholine; Hippocampus; Learning strategies; Memory modulation; Place learning; Response learning; Spatial learning; Striatum

Indexed keywords

ACETYLCHOLINE;

ACETYLCHOLINE RELEASE; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CONTROLLED STUDY; CORPUS STRIATUM; HIPPOCAMPUS; LEARNING; MALE; MAZE TEST; MEASUREMENT; MICRODIALYSIS; NEUROBIOLOGY; NONHUMAN; PREDICTION; RAT; TASK PERFORMANCE;

ACETYLCHOLINE; ANIMALS; CORPUS STRIATUM; HIPPOCAMPUS; INDIVIDUALITY; MALE; MAZE LEARNING; MICRODIALYSIS; RATS; RATS, SPRAGUE-DAWLEY; SPATIAL BEHAVIOR;

EID: 0037374222     PISSN: 10747427     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1074-7427(02)00014-X     Document Type: Article

References (46)

1. Bartus R.T., Dean R.L., Beer B., Lippa A.S. The cholinergic hypotheses of geriatric memory dysfunction. Science. 217:1982;408-417.
2. Barnes C.A., Nadel L., Honig W.K. Spatial memory deficit in senescent rats. Canadian Journal of Psychology. 34:1980;29-39.
3. Chang, Q., & Gold, P. E. (2002). Switching from hippocampal to striatal memory systems during learning: Changes in patterns of brain acetylcholine release in rats. Journal of Neuroscience (in press).
4. Cohen N.J., Squire L.R. Preserved learning and retention of pattern-analyzing skill in amnesia: Dissociation of knowing how and knowing that. Science. 210:1980;207-210.
5. Craik I.M., Salthouse T.A. The handbook of aging and cognition. 1992;Lawrence Erlbaum Associates, Hillsdale, NJ.
6. Daniel J.M., Dohanich G.P. Acetylcholine mediates the estrogen-induced increase in NMDA receptor binding in CA1 of the hippocampus and the associated improvement in working memory. Journal of Neuroscience. 21:2001;6949-6956.
7. Fadda F., Melis F., Stancampiano R. Increased hippocampal acetylcholine release during a working memory task. European Journal of Pharmacology. 307:1996;R1-R2.
8. Ferbinteanu J., McDonald R.J. Dorsal/ventral hippocampus, fornix, and conditioned place preference. Hippocampus. 11:2001;187-200.
9. Gabrieli J.D.E. Cognitive neuroscience of human memory. Annual Review of Psychology. 49:1998;87-115.
10. Gold P.E. Drug enhancement of memory in aged rodents and humans. Carroll M.E., Overmier J.B. Animal research and human health: Advancing human welfare through behavioral science. 2001;293-304 American Psychological Association, Washington, DC.
11. Gold P.E., McIntyre C., McNay E., Stefani M.R., Korol D.L. Neurochemical referees of dueling memory systems. Gold P.E., Greenough W.T. Memory consolidation: Essays in honor of James L. McGaugh - A time to remember. 2001;219-248 American Psychological Association Publishers, Washington, DC.
12. Grady C.L., Craik F.I. Changes in memory processing with age. Current Opinion in Neurobiology. 10:2000;224-231.
13. Kesner R.P. Neurobiological views of memory. Martinez J.L. Jr., Kesner R.P. Neurobiology of learning and memory. 1998;361-416 Academic Press, San Diego, CA.
14. Kesner R.P., Bolland B.L., Dakis M. Memory for spatial locations, motor responses, and objects: Triple dissociation among the hippocampus, caudate nucleus, and extrastriate visual cortex. Experimental Brain Research. 93:1993;462-470.
15. Kim J.J., Baxter M.G. Multiple brain-memory systems: The whole does not equal the sum of its parts. Trends in Neurosciences. 24:2001;324-330.
16. Korol D.L., Gold P.E. Glucose, memory and aging. The American Journal of Clinical Nutrition. 67:1998;764S-771S.
17. Korol D.L., Kolo L.L. Estrogen-induced changes in place and response learning in young adult female rats. Behavioral Neuroscience. 116:2002;411-420.
18. Korol D.L., Manning C.A. Effects of estrogen on cognition: Implications for menopause. Carroll M.E., Overmier J.B. Animal research and human health: Advancing human welfare through behavioral science. 2001;305-322 American Psychological Association Book Publisher, Washington, DC.
19. Matthews D.B., Best P.J. Fimbria/fornix lesions facilitate the learning of a nonspatial response task. Psychonomic Bulletin and Review. 2:1995;113-116.
20. Matthews D.B., Ilgen M., White A.M., Best P.J. Acute ethanol administration impairs spatial performance while facilitating nonspatial performance in rats. Neurobiology of Learning and Memory. 72:1999;169-179.
21. McDonald R.J., White N.M. Information acquired by the hippocampus interferes with acquisition of the amygdala-based conditioned-cue preference in the rat. Hippocampus. 5:1995;189-197.
22. McIntyre C.K., Pal S.N., Marriott L.K., Gold P.E. Competition between memory systems: Acetylcholine release in the hippocampus correlates negatively with good performance on an amygdala-dependent task. Journal of Neuroscience. 22:2002;1171-1176.
23. McIntyre, C. K., Marriott, L. K., & Gold, P. E. (2002b). Cooperation between memory systems: Acetylcholine release in the amygdala correlates positively with performance on a hippocampus-dependent task. Behavioral Neuroscience (in press).
24. Means L.W., Douglas R.J. Effects of hippocampal lesions on cue utilization in spatial discrimination in rats. Journal of Comparative and Physiological Psychology. 73:1970;254-260.
25. O'Keefe J.A., Nadel L. The hippocampus as a cognitive map. 1978;Oxford University Press, Oxford, England.
26. Packard M.G. Glutamate infused posttraining into the hippocampus or caudate-putamen differentially strengthens place and response learning. Proceedings of the National Academy of Sciences of the United States of America. 96:1999;12881-12886.
27. Packard M.G. Amygdala modulation of multiple memory systems. Gold P.E., Greenough W.T. Memory consolidation: Essays in honor of James L. McGaugh - A time to remember. 2001;201-218 American Psychological Association Publishers, Washington, DC.
28. Packard M.G., Cahill L.F., McGaugh J.L. Amygdala modulation of hippocampal-dependent and caudate nucleus-dependent memory processes. Proceedings of the National Academy of Sciences of the United States of America. 91:1994;8477-8481.
29. Packard M.G., McGaugh J.L. Inactivation of hippocampus or caudate nucleus with lidocaine differentially affects expression of place and response learning. Neurobiology of Learning and Memory. 65:1996;65-72.
30. Packard M.G., Teather L.A. Double dissociation of hippocampal and dorsal-striatal memory systems by posttraining intracerebral injections of 2-amino-5-phosphonopentanoic acid. Behavioral Neuroscience. 111:1997;543-551.
31. Packard M.G., Teather L.A. Amygdala modulation of multiple memory systems: Hippocampus and caudate-putamen. Neurobiology of Learning and Memory. 69:1998;163-203.
32. Pellegrino L.J., Pellegrino A.S., Cushman A.J. A stereotaxic atlas of the rat brain. 1979;Plenum, New York.
33. Poldrack R.A., Clark J., Pare-Blagoev E.J., Shohamy D., Moyano J.C., Myers C., Gluck M.A. Interactive memory systems in the human brain. Nature. 414:2001;546-550.
34. Powell D.A. A behavioral stages model of classical (Pavlovian) conditioning: Application to cognitive aging. Neuroscience & Biobehavioral Reviews. 23:1999;797-816.
35. Ragozzino M.E., Unick K.E., Gold P.E. Hippocampal acetylcholine release during memory testing in rats: Augmentation by glucose. Proceedings of the National Academy of Sciences of the United States of America. 93:1996;4693-4698.
36. Ragozzino M.E., Pal S.N., Unick K., Stefani M.R., Gold P.E. Modulation of hippocampal acetylcholine release and of memory by intrahippocampal glucose injections. Journal of Neuroscience. 18:1998;1595-1601.
37. Restle F. Discrimination of cues in mazes: A resolution of the "place-vs.-response" question. Psychological Review. 64:1957;217-228.
38. Stefani M.R., Gold P.E. Intrahippocampal infusions of k-atp channel modulators influence spontaneous alternation performance: Relationships to acetylcholine release in the hippocampus. Journal of Neuroscience. 21:2001;609-614.
39. Stoehr J.D., Mobley S.L., Roice D., Brooks R., Baker L.M., Wiley R.G., Wenk G.L. The effects of selective cholinergic basal forebrain lesions and aging upon expectancy in the rat. Neurobiology of Learning and Memory. 67:1997;214-227.
40. Suzuki M., Desmond T.J., Albin R.L., Frey K.A. Vesicular neurotransmitter transporters in Huntington's disease: Initial observations and comparison with traditional synaptic markers. Synapse. 41:2001;329-336.
41. Thiel C.M., Huston J.P., Schwarting R.K. Hippocampal acetylcholine and habituation learning. Neuroscience. 85:1998;1253-1262.
42. Tolman E.C., Ritchie B.F., Kalish D. Studies in spatial learning: II. Place learning versus response learning. Journal of Experimental Psychology. 35:1946;221-229.
43. White N.M., McDonald R.J. Acquisition of a spatial conditioned place preference is impaired by amygdala lesions and improved by fornix lesions. Behavioural Brain Research. 55:1993;269-281.
44. White N.M., McDonald R.J. Multiple parallel memory systems in the brain of the rat. Neurobiology of Learning and Memory. 77:2002;125-184.
45. Willingham D.B. A neuropsychological theory of motor skill learning. Psychological Review. 105:1998;558-584.
46. Woolley C.S. Estrogen-mediated structural and functional synaptic plasticity in the female rat hippocampus. Hormones and Behavior. 34:1998;140-148.