Cooperation between memory systems: Acetylcholine release in the amygdala correlates positively with performance on a hippocampus-dependent task

Behavioral Neuroscience

Volumn 117, Issue 2, 2003, Pages 320-326

  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

[No Author keywords available]

Indexed keywords

ACETYLCHOLINE;

ACETYLCHOLINE RELEASE; AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEPTH STIMULATION; HIPPOCAMPUS; LEARNING; MALE; MEMORY; MICRODIALYSIS; NONHUMAN; RAT; SPATIAL MEMORY; TASK PERFORMANCE; WORKING MEMORY;

ACETYLCHOLINE; AMYGDALA; ANIMALS; EXPLORATORY BEHAVIOR; HIPPOCAMPUS; MALE; MAZE LEARNING; MEMORY; MICRODIALYSIS; PSYCHOMOTOR PERFORMANCE; RATS; RATS, SPRAGUE-DAWLEY;

EID: 0037382109     PISSN: 07357044     EISSN: None     Source Type: Journal    
DOI: 10.1037/0735-7044.117.2.320     Document Type: Article

References (62)

1. Cahill, L. (2000). Modulation of long-term memory storage in humans by emotional arousal: Adrenergic activation and the amygdala. In J. P. Aggleton (Ed.), The amygdala: A functional analysis (2nd ed., pp. 425-445). New York: Oxford University Press.
2. Chang, Q., & Gold, P. E. (in press). Switching from hippocampal to striatal memory systems during learning: Changes in patterns of brain acetylcholine release in rats. Journal of Neuroscience.
3. Dalmaz, C., Introini-Collison, I. B., & McGaugh, J. L. (1993). Noradrenergic and cholinergic interactions in the amygdala and the modulation of memory storage. Behavioural Brain Research, 58, 167-174.
4. Darnaudéry, M., Koehl, M., Piazza, P. V., Le Moal, M., & Mayo, W. (2000). Pregnenolone sulfate increases hippocampal acetylcholine release and spatial recognition. Brain Research, 852, 173-179.
5. Davis, M. (1992). The role of the amygdala in conditioned fear. In J. P. Aggleton (Ed.), The amygdala: Neurobiological aspects of emotion, memory and mental dysfunction (pp. 255-306). New York: Wiley-Liss.
6. Disterhoft, J. F., Kronforst-Collins, M., Oh, M. M., Power, J. M., Preston, A. R., & Weiss, C. (1999). Cholinergic facilitation of trace eyeblink conditioning in aging rabbits. Life Sciences, 64, 541-548.
7. Fadda, F., Cocco, S., & Stancampiano, R. (2000). Hippocampal acetylcholine release correlates with spatial learning performance in freely moving rats. NeuroReport, 11, 2265-2269.
8. Fadda, F., Melis, F., & Stancampiano, R. (1996). Increased hippocampal acetylcholine release during a working memory task. European Journal of Pharmacology, 307, R1-R2.
9. Ferbinteanu, J., & McDonald, R. J. (2001). Dorsal/ventral hippocampus, fornix, and conditioned place preference. Hippocampus, 11, 187-200.
10. Gabrieli, J. D. E. (1998). Cognitive neuroscience of human memory. Annual Review of Psychology, 49, 87-115.
11. Gold, P. E. (1995). Modulation of emotional and non-emotional memories: Same pharmacological system, different neuroanatomical systems. In J. L. McGaugh, N. M. Weinberger, & G. S. Lynch (Eds.), Brain and memory: Modulation and mediation of neuroplasticity (pp. 41-74). New York: Oxford University Press.
12. Gold, P. E., & McGaugh, J. L. (1975). A single-trace, two-process view of memory storage processes. In D. Deutsch & J. A. Deutsch (Eds.), Short-term memory (pp. 355-378). New York: Academic Press.
13. Gold, P. E., McIntyre, C., McNay, E., Stefani, M. R., & Korol, D. L. (2001). Neurochemical referees of dueling memory systems. In P. E. Gold & W. T. Greenough (Eds.), Memory consolidation: Essays in honor of James L. McGaugh - A time to remember (pp. 219-248). Washington, DC: American Psychological Association.
14. Hiramatsu, M., Murasawa, H., Mori, H., & Kameyama, T. (1998). Reversion of muscarinic autoreceptor agonist-induced acetylcholine decrease and learning impairment by dynorphin A (1-13), an endogenous kappaopioid receptor agonist. British Journal of Pharmacology, 123, 920-926.
15. Hiramatsu, M., Murasawa, H., Nabeshima, T., & Kameyama, T. (1998). Effects of U-50,488H on scopolamine-, mecamylamine- and dizocilpine-induced learning and memory impairment in rats. Journal of Pharmacology and Experimental Therapeutics, 284, 858-867.
16. Hironaka, N., Tanaka, K., Izaki, Y., Hori, K., & Nomura, M. (2001). Memory-related acetylcholine efflux from rat prefrontal cortex and hippocampus: A microdialysis study. Brain Research, 901, 143-150.
17. Hirsh, R. (1974). The hippocampus and contextual retrieval of information from memory: A theory. Behavioural Biology, 12, 421-444.
18. Ikegaya, Y., Saito, H., & Abe K. (1996a). The basomedial and basolateral amygdaloid nuclei contribute to the induction of long-term potentiation in the dentate gyrus in vivo. European Journal of Neuroscience, 8, 1833-1839.
19. Ikegaya, Y., Saito, H., & Abe, K. (1996b). Dentate gyrus field potentials evoked by stimulation of the basolateral amygdaloid nucleus in anesthetized rats. Brain Research, 718, 53-60.
20. Ingram, D. K., Spangler, E. L., Iijima, S., Ikari, H., Kuo, H., Greig, N. H., & London, E. D. (1994). Rodent models of memory dysfunction in Alzheimer's disease and normal aging: Moving beyond the cholinergic hypothesis. Life Sciences, 55, 2037-2049.
21. Introini-Collison, I. B., Dalmaz, C., & McGaugh, J. L. (1996). Amygdala beta-noradrenergic influences on memory storage involve cholinergic activation. Neurobiology of Learning and Memory, 65, 57-64.
22. Kesner, R. P., Gilbert, P. E., & Lee, I. (2002). Subregional analysis of hippocampal function in the rat. In L. R. Squire & D. L. Schacter (Eds.), Neuropsychology of memory (pp. 395-1411). New York: Guilford Press.
23. Kobayashi, T., & Iwasaki, T. (2000). Functional dissociation of striatal and hippocampal cholinergic systems in egocentric and allocentric localization: Effect of overtraining. Nihon Shinkei Seishin Yakurigaku Zasshi, 20, 113-121.
24. Kopf, S., Buchholzer, M., Hilgert, M., Löffelholz, K., & Klein, J. (2001). Glucose plus choline improve passive avoidance behavior and increase hippocampal acetylcholine release in mice. Neuroscience, 103, 365-371.
25. LeDoux, J. E. (2000). Emotion circuits in the brain. Annual Review of Neuroscience, 23, 155-184.
26. Levin, E. D., & Simon, B. B. (1998). Nicotinic acetylcholine involvement in cognitive function in animals. Psychopharmacology (Berlin), 138, 217-230.
27. Matthews, D. B., & Best, P. J. (1995). Fimbria/fornix lesions facilitate the learning of a nonspatial response task. Psychonomic Bulletin and Review, 2, 113-116.
28. Matthews, D. B., Ilgen, M., White, A. M., & Best, P. J. (1999). Acute ethanol administration impairs spatial performance while facilitating nonspatial performance in rats. Neurobiology of Learning and Memory, 72, 169-79.
29. McDonald, R. J., & White, N. M. (1995). Information acquired by the hippocampus interferes with acquisition of the amygdala-based conditioned-cue preference in the rat. Hippocampus, 5, 189-197.
30. McGaugh, J. L., Cahill, L., & Roozendaal, B. (1996). Involvement of the amygdala in memory storage: Interaction with other brain systems. Proceedings of the National Academy of Sciences, USA, 93, 13508-13514.
31. McGaugh, J. L. (2000, January 14). Memory - a century of consolidation. Science, 287, 248-251.
32. McIntyre, C. K., Marriott, L. K., & Gold, P. E. (2003). Patterns of brain acetylcholine release predict differences in learning strategies used by individual rats. Neurobiology of Learning and Memory, 79, 177-183.
33. McIntyre, C. K., Pal, S. N., Marriott, L. K., & Gold, P. E. (2002). Competition between memory systems: Acetylcholine release in the hippocampus correlates negatively with good performance on an amygdala-dependent task. Journal of Neuroscience, 22, 1171-1176.
34. McIntyre, C. K., Ragozzino, M. E., & Gold, P. E. (1998). Intra-amygdala infusions of scopolamine impair performance on a conditioned place preference task but not a spatial radial maze task. Behavioural Brain Research, 95, 219-226.
35. McNay, E. C., & Gold, P. E. (1998). Memory modulation across neural systems: Intra-amygdala glucose reverses deficits caused by intraseptal morphine on a spatial task but not on an aversive task. Journal of Neuroscience, 18, 3853-3858.
36. McNay, E. C., & Gold, P. E. (1999). Extracellular glucose concentrations in the rat hippocampus measured by zero-net-flux: Effects of microdialysis flow rate, strain, and age. Journal of Neurochemistry, 72, 785-790.
37. Nyberg, L., & Tulving, E. (1996). Classifying human long-term memory: Evidence from converging dissociations. European Journal of Cognitive Psychology, 8, 163-183.
38. O'Keefe, J., & Nadel, L. (1978). The hippocampus as a cognitive map. Oxford, England: Oxford University Press.
39. Packard, M. G. (2001a). Amygdala modulation of multiple memory systems. In P. E. Gold & W. T. Greenough (Eds.), Memory consolidation: Essays in honor of James L. McGaugh - A time to remember (pp. 201-218). Washington, DC: American Psychological Association.
40. Packard, M. G. (2001b). On the neurobiology of multiple memory systems: Tolman versus Hull, system interactions, and the emotion-memory link. Journal of Cognitive Processing, 2, 1-22.
41. Packard, M. G., Cahill, L. F., & McGaugh, J. L. (1994). Amygdala modulation of hippocampal-dependent and caudate nucleus-dependent memory processes. Proceedings of the National Academy of Sciences, USA, 91, 8477-8481.
42. Packard, M. G., Hirsh, R., & White, N. M. (1989). Differential effects of fornix and caudate nucleus lesions on two radial maze tasks: Evidence for multiple memory systems. Journal of Neuroscience, 9, 1465-1472.
43. Packard, M. G., & Teather, L. A. (1998). Amygdala modulation of multiple memory systems: Hippocampus and caudate-putamen. Neurobiology of Learning and Memory, 69, 163-203.
44. Passani, M. B., Cangioli, I., Baldi, E., Bucherelli, C., Mannaioni, P. F., & Blandina, P. (2001). Histamine H3 receptor-mediated impairment of contextual fear conditioning and in-vivo inhibition of cholinergic transmission in the rat basolateral amygdala. European Journal of Neuroscience, 14, 1522-1532.
45. Pellegrino, L. J., Pellegrino, A. S., & Cushman, A. J. (1979). A stereotaxic atlas of the rat brain. New York: Plenum Press.
46. Power, A. E., & McGaugh, J. L. (2002). Pthalic acid amygdalopetal lesion of the nucleus basalis magnocellularis induces reversible memory deficits in rats. Neurobiology of Learning and Memory, 77, 322-388.
47. Power, A. E., Roozendaal, B., & McGaugh, J. L. (2000). Glucocorticoid enhancement of memory consolidation in the rat is blocked by muscarinic receptor antagonism in the basolateral amygdala. European Journal of Neuroscience, 12, 3481-3487.
48. Ragozzino, M. E., & Gold, P. E. (1995). Glucose injections into the medial septum reverse the effects of intraseptal morphine infusions on hippocampal acetylcholine output and memory. Neuroscience, 68, 981-988.
49. Ragozzino, M. E., & Kesner, R. P. (1998). The effects of muscarinic cholinergic receptor blockade in the rat anterior cingulate and prelimbic/infralimbic cortices on spatial working memory. Neurobiology of Learning and Memory, 69, 241-257.
50. Ragozzino, M. E., Pal, S. N., Unick, K., Stefani, M. R., & Gold, P. E. (1998). Modulation of hippocampal acetylcholine release and spontaneous alternation scores by intrahippocampal glucose injections. Journal of Neuroscience, 18, 1595-1601.
51. Ragozzino, M. E., Unick, K. E., & Gold, P. E. (1996). Hippocampal acetylcholine release during memory testing in rats: Augmentation by glucose. Proceedings of the National Academy of Science, USA, 93, 4693-4698.
52. Riedel, W. J., & Jolles, J. (1996). Cognition enhancers in age-related cognitive decline. Drugs and Aging, 8, 245-274.
53. Roozendaal, B., & McGaugh, J. L. (1997). Basolateral amygdala lesions block the memory-enhancing effect of glucocorticoid administration in the dorsal hippocampus of rats. European Journal of Neuroscience, 9, 76-83.
54. Schildein, S., Huston, J. P., & Schwarting, R. K. (2000). Injections of tacrine and scopolamine into the nucleus accumbens: Opposing effects of immediate vs delayed posttrial treatment on memory of an open field. Neurobiology of Learning and Memory, 73, 21-30.
55. Squire, L. R., Knowlton, B., & Musen, G. (1993). The structure and organization of memory. Annual Review of Psychology, 44, 453-495.
56. Stefani, M. R., & Gold, P. E. (1998). Intra-septal injections of glucose and glibenclamide attenuate galanin-induced spontaneous alternation performance deficits in the rat. Brain Research, 813, 50-56.
57. Thiel, C., Huston, J., & Schwarting, R. (1998). Hippocampal acetylcholine and habituation learning. Neuroscience, 85, 1253-1262.
58. Wallenstein, G. V., & Vago, D. R. (2001). Intrahippocampal scopolamine impairs both acquisition and consolidation of contextual fear conditioning. Neurobiology of Learning and Memory, 75, 245-252.
59. Weiskrantz, L. (1956). Behavioral changes associated with ablation of the amygdaloid complex in monkeys. Journal of Comparative Physiology and Psychology, 49, 381-391.
60. White, N. M., & McDonald R. J. (1993). Acquisition of a spatial conditioned place preference is impaired by amygdala lesions and improved by fornix lesions. Behavioural Brain Research, 55, 269-281.
61. White, N. M., & McDonald, R. J. (2002). Multiple parallel memory systems in the brain of the rat. Neurobiology of Learning and Memory, 77, 125-184.
62. Willingham, D. B. (1997). Systems of memory in the human brain. Neuron, 18, 5-8.