Acetylcholine release in the hippocampus and striatum during place and response training

Learning and Memory

Volumn 12, Issue 6, 2005, Pages 564-572

  Pych, Jason C ^a   Chang, Qing ^a   Colon Rivera, Cynthia ^a   Haag, Renee ^a   Gold, Paul E ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCHOLINE;

ACETYLCHOLINE RELEASE; ANIMAL BEHAVIOR; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASSOCIATION; CONTROLLED STUDY; CORPUS STRIATUM; EXTRACELLULAR FLUID; FOOD INTAKE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HIPPOCAMPUS; MAZE TEST; MICRODIALYSIS; NONHUMAN; PLACE PREFERENCE; PRIORITY JOURNAL; RAT; RESPONSE TIME; REWARD; SPATIAL FREQUENCY DISCRIMINATION; SPECIES COMPARISON; STATE DEPENDENT LEARNING; TASK PERFORMANCE;

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

EID: 28844460333     PISSN: 10720502     EISSN: 15495485     Source Type: Journal    
DOI: 10.1101/lm.33105     Document Type: Article

References (80)

1. Adams, S.V., Winterer, J., and Muller, W. 2004. Muscarinic signaling is required for spike-pairing induction of long-term potentiation at rat Schaffer collateral-CA1 synapses. Hippocampus 14: 413-416.
2. Berkeley, J.L., Gomeza, J., Wess, J., Hamilton, S.E., Nathanson, N.M., and Levey, A.I. 2001. M1 muscarinic acetylcholine receptors activate extracellular signal-regulated kinase in CA1 pyramidal neurons in mouse hippocampal slices. Mol. Cell. Neurosci. 18: 512-524.
3. Carli, M., Luschi, R., and Samanin, R. 1997. Dose-related impairment of spatial learning by intrahippocampal scopolamine: Antagonism by ondansetron, a 5-HT3 receptor antagonist. Behav. Brain Res. 82: 185-194.
4. Chang, Q. and Gold, P.E. 2003. Switching memory systems during learning: Changes in patterns of brain acetylcholine release in the hippocampus and striatum in rats. J. Neurosci. 23: 3001-3005.
5. -. 2004. Inactivation of dorsolateral striatum impairs acquisition of response learning in cue-deficient, but not cue-available, conditions. Behav. Neurosci. 118: 383-388.
6. Cohen, N.J. and Squire, L.R. 1980. Preserved learning and retention of pattern-analyzing skill in amnesia: Dissociation of knowing how and knowing that. Science 210: 207-210.
7. Colombo, P.J. 2004. Learning-induced activation of transcription factors among multiple memory systems. Neurobiol. Learn. Mem. 82: 268-277.
8. Colombo, P.J., Brightwell, J.J., and Countryman, R.A. 2003. Cognitive strategy-specific increases in phosphorylated cAMP response element-binding protein and c-Fos in the hippocampus and dorsal striatum. J. Neurosci. 23: 3547-3554.
9. Degroot, A. and Parent, M.B. 2000. Increasing acetylcholine levels in the hippocampus or entorhinal cortex reverses the impairing effects of septal GABA receptor activation on spontaneous alternation. Learn. Mem. 7: 293-302.
10. Diaz del Guante, M.A., Carbonell-Hernandez, C., Quirarte, G., Cruz-Morales, S.E., Rivas-Arancibia, S., and Prado-Alcala, R.A. 1993. Intrastriatal injection of choline accelerates the acquisition of positively rewarded behaviors. Brain Res. Bull. 30: 671-675.
11. Dineley, K.T., Westerman, M., Bui, D., Bell, K., Ashe, K.H., and Sweatt, J.D. 2001. β-Amyloid activates the mitogen-activated protein kinase cascade via hippocampal α7 nicotinic acetylcholine receptors: In vitro and in vivo mechanisms related to Alzheimer's disease. J. Neurosci. 21: 4125-4133.
12. Disterhoft, J.F. and Matthew, Oh M. 2003. Modulation of cholinergic transmission enhances excitability of hippocampal pyramidal neurons and ameliorates learning impairments in aging animals. Neurobiol. Learn. Mem. 80: 223-233.
13. Dutar, P., Bassant, M.H., Senut, M.C., and Lamour, Y. 1995. The septohippocampal pathway: Structure and function of a central cholinergic system. Physiol. Rev. 75: 393-427.
14. Farr, S.A., Uezu, K., Flood, J.F., and Morley, J.E. 1999. Septo-hippocampal drug interactions in post-trial memory processing. Brain Res. 847: 221-230.
15. Farr, S.A., Flood, J.F., and Morley, J.E. 2000. The effect of cholinergic, GABAergic, serotonergic, and glutamatergic receptor modulation on posttrial memory processing in the hippocampus. Neurobiol. Learn. Mem. 73: 150-167.
16. Ferreira, A.R., Furstenau, L., Blanco, C., Kornisiuk, E., Sanchez, G., Daroit, D., Castro e Silva, M., Cervenansky, C., Jerusalinsky, D., and Quillfeldt, J.A. 2003. Role of hippocampal M1 and M4 muscarinic receptor subtypes in memory consolidation in the rat. Pharmacol. Biochem. Behav. 74: 411-415.
17. Frotscher, M. and Leranth, C. 1985. Cholinergic innervation of the rat hippocampus as revealed by choline acetyltransferase immunocytochemistry: A combined light and electron microscopic study. J. Comp. Neurol. 239: 237-246.
18. Gillette, M.U. and Mitchell, J.W. 2002. Signaling in the suprachiasmatic nucleus: Selectively responsive and integrative. Cell Tissue Res. 309: 99-107.
19. Gold, P.E. 2003. Acetylcholine modulation of neural systems involved in learning and memory. Neurobiol. Learn. Mem. 80: 194-210.
20. -. 2004. Coordination of multiple memory systems. Neurobiol. Learn. Mem. 82: 230-242.
21. Gold, P.E., McIntyre, C.K., McNay, E.C., Stefani, M.R., and Korol, D.L. 2001. Neurochemical referees of dueling memory systems. In Essays in honor of James L. McGaugh (eds. P.E. Gold and W.T. Greenough), pp. 219-248. American Psychological Press, Washington, DC.
22. Graybiel, A.M. 1995. The basel ganglia. Tr. Neurosci. 18: 60-62.
23. Greenberg, M.E., Ziff, E.B., and Greene, L.A. 1986. Stimulation of neuronal acetylcholine receptors induces rapid gene transcription. Science 234: 80-83.
24. Greenwood, J.M. and Dragunow, M. 2002. Muscarinic receptor-mediated phosphorylation of cyclic AMP response element binding protein in human neuroblastoma cells. J. Neurochem. 82: 389-397.
25. Gu, Q. 2002. Neuromodulatory transmitter systems in the cortex and their role in cortical plasticity. Neuroscience 111: 815-835.
26. Hasselmo, M.E. 1995. Neuromodulation and cortical function: Modeling the physiological basis of behavior. Behav. Brain Res. 67: 1-27.
27. Hasselmo, M.E. and McGaughy, J. 2004. High acetylcholine levels set circuit dynamics for attention and encoding and low acetylcholine levels set dynamics for consolidation. Prog. Brain Res. 145: 207-231.
28. Hu, M., Liu, Q.S., Chang, K.T., and Berg, D.K. 2002. Nicotinic regulation of CREB activation in hippocampal neurons by glutamatergic and nonglutamatergic pathways. Mol. Cell. Neurosci. 21: 616-625.
29. Izquierdo, I., da Cunha, C., Rosat, R., Jerusalinsky, D., Ferreira, M.B., and Medina, J.H. 1992. Neurotransmitter receptors involved in post-training memory processing by the amygdala, medial septum, and hippocampus of the rat. Behav. Neural Biol. 58: 16-26.
30. Kesner, R.P., Bolland, B.L., and Dakis, M. 1993. Memory for spatial locations, motor responses, and objects: Triple dissociation among the hippocampus, caudate nucleus, and extrastriate visual cortex. Exp. Brain Res. 93: 462-470.
31. Kim, J.S. and Levin, E.D. 1996. Nicotinic, muscarinic and dopaminergic actions in the ventral hippocampus and the nucleus accumbens: Effects on spatial working memory in rats. Brain Res. 725: 231-240.
32. Kobayashi, T. and 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.
33. Lazaris, A., Cassel, S., Stemmelin, J., Cassel, J.C., and Kelche, C. 2003. Intrastriatal infusions of methoctramine improve memory in cognitively impaired aged rats. Neurobiol. Aging 24: 379-383.
34. Masuda, Y. and Iwasaki, T. 1984. Effects of caudate lesions on radial maze behavior in rats. Jpn. Psychol. Res. 26: 42-49.
35. McDonald, R.J. and White, N.M. 1993. A triple dissociation of memory systems: Hippocampus, amygdala, and dorsal striatum. Behav. Neurosci. 107: 3-22.
36. -. 1995. Information acquired by the hippocampus interferes with acquisition of the amygdala-based conditioned-cue preference in the rat. Hippocampus 5: 189-197.
37. McIntyre, C.K., Pal, S.N., Marriott, L.K., and Gold, P.E. 2002. Competition between memory systems: Acetylcholine release in the hippocampus correlates negatively with good performance on an amygdala-dependent task. J. Neurosci. 22: 1171-1176.
38. McIntyre, C.K., Marriott, L.K., and Gold, P.E. 2003a. Cooperation between memory systems: Acetylcholine release in the amygdala correlates positively with performance on a hippocampus-dependent task. Behav. Neurosci. 117: 320-326.
39. -. 2003b. Patterns of brain acetylcholine release predict individual differences in preferred learning strategies in rats. Neurobiol. Learn. Mem. 79: 177-183.
40. McNay, E.C. and Gold, P.E. 1999. Extracellular glucose concentrations in the rat hippocampus measured by zero-net-flux: Effects of microdialysis flow rate, strain, and age. J. Neurochem. 72: 785-790.
41. McNay, E.C., McCarty, R.C., and Gold, P.E. 2001. Fluctuations in brain glucose concentration during behavioral testing: Dissociations between brain areas and between brain and blood. Neurobiol. Learn. Mem. 75: 325-337.
42. Mesulam, M.M., Mufson, E.J., Wainer, B.H., and Levey, A.I. 1983. Central cholinergic pathways in the rat: An overview based on an alternative nomenclature (Ch1-Ch6). Neurosci. 10: 1185-1201.
43. Mitchell, J.A. and Hall, G. 1988. Caudate-putamen lesions in the rat may impair or potentiate maze learning depending upon availability of stimulus cues and relevance of response cues. Q.J. Exp. Psychol. B 40: 243-258.
44. Mizumori, S.J., Yeshenko, O., Gill, K.M., and Davis, D.M. 2004. Parallel processing across neural systems: Implications for a multiple memory system hypothesis. Neurobiol. Learn. Mem. 82: 278-298.
45. Moser, M.B. and Moser, E.I. 1998. Functional differentiation in the hippocampus. Hippocampus 8: 608-619.
46. Ohno, M., Yamamoto, T., and Watanabe, S. 1994. Blockade of hippocampal M1 muscarinic receptors impairs working memory performance of rats. Brain Res. 650: 260-266.
47. Packard, M.G. and Cahill, L. 2001. Affective modulation of multiple memory systems. Curr. Opin. Neurobiol. 11: 752-756.
48. Packard, M.G. and McGaugh, J.L. 1992. Double dissociation of fornix and caudate nucleus lesions on acquisition of two water maze tasks: Further evidence for multiple memory systems. Behav. Neurosci. 106: 439-446.
49. -. 1996. Inactivation of hippocampus or caudate nucleus with lidocaine differentially affects expression of place and response learning. Neurobiol. Learn. Mem. 65: 65-72.
50. Packard, M.G., Hirsh, R., and White, N.M. 1989. Differential effects of fornix and caudate nucleus lesions on two radial maze tasks: Evidence for multiple memory systems. J. Neurosci. 9: 1465-1472.
51. Paxinos, G. and Watson, C. 1986. The rat brain in stereotaxic coordinates. Academic Press, New York.
52. Poldrack, R.A. and Packard, M.G. 2003. Competition among multiple memory systems: Converging evidence from animal and human brain studies. Neuropsychologia 41: 245-251.
53. Pollack, A.E. 2001. Anatomy, physiology, and pharmacology of the basal ganglia. Neurologic Clin. 19: 523-534.
54. Power, A.E., Vazdarjanova, A., and McGaugh, J.L. 2003. Muscarinic cholinergic influences in memory consolidation. Neurobiol. Learn. Mem. 80: 178-193.
55. Prado-Alcala, R.A. 1985. Is cholinergic activity of the caudate nucleus involved in memory? Life Sci. 37: 2135-2142.
56. Prado-Alcala, R.A., Cruz-Morales, S.E., and Lopez-Miro, F.A. 1980. Differential effects of cholinergic blockade of anterior and posterior caudate nucleus on avoidance behaviors. Neurosci. Lett. 18: 339-345.
57. Prado-Alcala, R.A., Cepeda, G., Verduzco, L., Jimenez, A., and Vargas-Ortega, E. 1984. Effects of cholinergic stimulation of the caudate nucleus on active avoidance. Neurosci. Lett. 51: 31-36.
58. Prado-Alcala, R.A., Fernandez-Samblancat, M., and Solodkin-Herrera, M. 1985. Injections of atropine into the caudate nucleus impair the acquisition and the maintenance of passive avoidance. Pharmacol. Biochem. Behav. 22: 243-247.
59. Pych, J.C., Chang, Q., Colon-Rivera, C., and Gold, P.E. 2005. Acetylcholine release in hippocampus and striatum during testing on a rewarded spontaneous alternation task. Neurobiol. Learn. Mem. 84: 93-101.
60. Ragozzino, M.E. 2003. Acetylcholine actions in the dorsomedial striatum support the flexible shifting of response patterns. Neurobiol. Learn. Mem. 80: 257-267.
61. Ragozzino, M.E., Wenk, G.L., and Gold, P.E. 1994. Glucose attenuates a morphine-induced decrease in hippocampal acetylcholine output: An in vivo microdialysis study in rats. Brain Res. 655: 77-82.
62. Ragozzino, M.E., Unick, K.E., and Gold, P.E. 1996. Hippocampal acetylcholine release during memory testing in rats: Augmentation by glucose. Proc. Natl. Acad. Sci. 93: 4693-4698.
63. Ragozzino, M.E., Pal, S.N., Unick, K., Stefani, M.R., and Gold, P.E. 1998. Modulation of hippocampal acetylcholine release and spontaneous alternation scores by intrahippocampal glucose injections. J. Neurosci. 18: 1595-1601.
64. Restle, F. 1957. Discrimination of cues in mazes: A resolution of the place-vs.-response question. Psychol. Rev. 64: 217-228.
65. Riekkinen Jr., P., Schmidt, B., and Riekkinen, M. 1997. Behavioral characterization of metrifonate-improved acquisition of spatial information in medial septum-lesioned rats. Eur. J. Pharmacol. 323: 11-19.
66. Rogers, J.L. and Kesner, R.P. 2004. Cholinergic modulation of the hippocampus during encoding and retrieval of tone/shock-induced fear conditioning. Learn. Mem. 11: 102-107.
67. Rosenblum, K., Futter, M., Jones, M., Hulme, E.C., and Bliss, T.V. 2000. ERKI/II regulation by the muscarinic acetylcholine receptors in neurons. J. Neurosci. 20: 977-985.
68. Rossi, M.A., Mash, D.C., and deToledo-Morrell, L. 2005. Spatial memory in aged rats is related to PKCγ-dependent G-protein coupling of the M1 receptor. Neurobiol. Aging 26: 53-68.
69. Sarter, M., Bruno, J.P., and Givens, B. 2003. Attentional functions of cortical cholinergic inputs: What does it mean for learning and memory? Neurobiol. Learn. Mem. 80: 245-256.
70. Sarter, M., Hasselmo, M.E., Bruno, J.P., and Givens, B. 2005. Unraveling the attentional functions of cortical cholinergic inputs: Interactions between signal-driven and cognitive modulation of signal detection. Brain Res. Brain Res. Rev. 48: 98-111.
71. Segal, M. and Auerbach, J.M. 1997. Muscarinic receptors involved in hippocampal plasticity. Life Sci. 60: 1085-1091.
72. Teather, L.A., Packard, M.G., Smith, D.E., Ellis-Behnke, R.G., and Bazan, N.G. 2005. Differential induction of c-Jun and Fos-like proteins in rat hippocampus and dorsal striatum after training in two water maze tasks. Neurobiol. Learn. Mem. 84: 75-84.
73. Tolman, E.C. 1948. Cognitive maps in rats and men. Psych. Rev. 55: 189-208.
74. Tzavos, A., Jih, J., and Ragozzino, M.E. 2004. Differential effects of M1 muscarinic receptor blockade and nicotinic receptor blockade in the dorsomedial striatum on response reversal learning. Behav. Brain Res. 154: 245-253.
75. Wagner, A.D., Schacter, D.L., Rotte, M., Koutstaal, W., Maril, A., Dale, A.M., Rosen, B.R., and Buckner, R.L. 1998. Building memories: Remembering and forgetting of verbal experiences as predicted by brain activity. Science 281: 1188-1191.
76. Weinberger, N.M. 2003. The nucleus basalis and memory codes: Auditory cortical plasticity and the induction of specific, associative behavioral memory. Neurobiol. Learn. Mem. 80: 268-284.
77. -. 2004. Specific long-term memory traces in primary auditory cortex. Nat. Rev. Neurosci. 5: 279-290.
78. Weiss, C., Preston, A.R., Oh, M.M., Schwarz, R.D., Welty, D., and Disterhoft, J.F. 2000. The M1 muscarinic agonist CI-1017 facilitates trace eyeblink conditioning in aging rabbits and increases the excitability of CA1 pyramidal neurons. J. Neurosci. 20: 783-790.
79. Westerink, B.H. and Timmerman, W. 1999. Do neurotransmitters sampled by brain microdialysis reflect functional release? Anal. Chim. Acta 373: 263-274.
80. White, N.M. and McDonald, R.J. 2002. Multiple parallel memory systems in the brain of the rat. Neurobiol. Learn. Mem. 77: 125-184.