Acetylcholine modulation of neural systems involved in learning and memory

Neurobiology of Learning and Memory

Volumn 80, Issue 3, 2003, Pages 194-210

  Gold, Paul E ^a  

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

Author keywords

Acetylcholine; Amygdala; Hippocampus; Learning; Memory; Microdialysis; Multiple memory systems; Septohippocampal; Spatial working memory; Striatum

Indexed keywords

ACETYLCHOLINE;

ACETYLCHOLINE RELEASE; CHOLINERGIC SYSTEM; CONFERENCE PAPER; HUMAN; LEARNING; MEMORY; MEMORY DISORDER; MICRODIALYSIS; NERVOUS SYSTEM; NONHUMAN; REGULATORY MECHANISM; TASK PERFORMANCE; TRAINING;

EID: 0141522452     PISSN: 10747427     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nlm.2003.07.003     Document Type: Conference Paper

References (177)

1. Aloisi A.M., Casamenti F., Scali C., Pepeu G., Carli G. Effects of novelty, pain and stress on hippocampal extracellular acetylcholine levels in male rats. Brain Research. 748:1997;219-226.
2. Alreja M., Wu M., Liu W., Atkins J.B., Leranth C., Shanabrough M. Muscarinic tone sustains impulse flow in the septohippocampal GABA but not cholinergic pathway: Implications for learning and memory. Journal of Neuroscience. 20:2000;8103-8110.
3. Arnold H., Burk J., Hodgson E., Sarter M., Bruno J. Differential cortical acetylcholine release in rats performing a sustained attention task versus behavioral control tasks that do not explicitly tax attention. Neuroscience. 114:2002;451-460.
4. Bartus R.T., Dean R.L. III, Beer B., Lippa A.S. The cholinergic hypothesis of geriatric memory dysfunction. Science. 217:1982;408-417.
5. Baxter M.G., Bucci D.J., Gorman L.K., Wiley R.G., Gallagher M. Selective immunotoxic lesions of basal forebrain cholinergic cells: Effects on learning and memory in rats. Behavioral Neuroscience. 109:1995;714-722.
6. Baxter M.G., Bucci D.J., Sobel T.J., Williams M.J., Gorman L.K., Gallagher M. Intact spatial learning following lesions of basal forebrain cholinergic neurons. Neuroreport. 7:1996;1417-1420.
7. Baxter M.G., Gallagher M. Intact spatial learning in both young and aged rats following selective removal of hippocampal cholinergic input. Behavioral Neuroscience. 110:1996;460-467.
8. Baxter M.G., Murg S. The basal forebrain cholinergic system and memory: Beware of dogma. Squire L., Schacter D. Neuropsychology of memory. 2002;425-436 Guilford Press, New York.
9. Beylin A.V., Shors T.J. Glucocorticoids are necessary for enhancing the acquisition of associative memories after acute stressful experience. Hormones and Behavior. 43:2003;124-131.
10. Bizon J.L., Han J.-S., Hudon C., Gallagher M. Effects of hippocampal cholinergic deafferentation on learning strategy selection in a visible platform version of the water maze. Hippocampus. 13:2003;676-684.
11. Bjordahl T.S., Dimyan M.A., Weinberger N.M. Induction of long-term receptive field plasticity in the auditory cortex of the waking guinea pig by stimulation of the nucleus basalis. Behavioral Neuroscience. 112:1998;467-479.
12. Bowman R.E., Beck K.D., Luine V.N. Chronic stress effects on memory: Sex differences in performance and monoaminergic activity. Hormones and Behavior. 43:2003;48-59.
13. Bruno J.P., Sarter M., Arnold H., Himmelheber A.M. In vivo neurochemical correlates of cognitive processes: Methodological and conceptual challenges. Reviews in the Neurosciences. 10:1999;25-48.
14. Cahill J.F., Baxter M.G. Cholinergic and noncholinergic septal neurons modulate strategy selection in spatial learning. European Journal of Neuroscience. 14:2001;1856-1864.
15. Carli M., Luschi R., Samanin R. Dose-related impairment of spatial learning by intrahippocampal scopolamine: Antagonism by ondansetron, a 5-HT3 receptor antagonist. Behavioural Brain Research. 82:1997;185-194.
16. Chang, Q., & Gold, P. E. (2003a). Impaired and spared cholinergic functions in the hippocampus after lesions of the medial septum/ventral diagonal band with 192 IgG-saporin. Hippocampus, in press.
17. Chang, Q., & Gold, P. E. (2003b). Intra-hippocampal lidocaine injections impair acquisition of a place task and facilitate acquisition of a response task in rats. Behavioural Brain Research, in press.
18. Chang Q., Gold P.E. Switching from hippocampal to striatal memory systems during learning: Changes in patterns of acetylcholine release in rats. Journal of Neuroscience. 23:2003;3001-3005.
19. Chappell J., McMahan R., Chiba A., Gallagher M. A re-examination of the role of basal forebrain cholinergic neurons in spatial working memory. Neuropharmacology. 37:1998;481-487.
20. Conrad C.D., Grote K.A., Hobbs R.J., Ferayorni A. Sex differences in spatial and non-spatial Y-maze performance after chronic stress. Neurobiology of Learning and Memory. 79:2003;32-40.
21. Coyle J.T., Price D.L., DeLong M.R. Alzheimer's disease: A disorder of the cortical cholinergic innervation. Science. 219:1983;1184-1190.
22. Darnaudery M., Koehl M., Piazza P.V., Le Moal M., Mayo W. Pregnenolone sulfate increases hippocampal acetylcholine release and spatial recognition. Brain Research. 852:2000;173-179.
23. Day J.C., Kornecook T.J., Quirion R. Application of in vivo microdialysis to the study of cholinergic systems. Methods. 23:2001;21-39.
24. Decker M.W., Radek R.J., Majchrzak M.J., Anderson D.J. Differential effects of medial septal lesions on spatial-memory tasks. Psychobiology. 20:1992;9-17.
25. Degroot A., Parent M.B. Increasing acetylcholine levels in the hippocampus or entorhinal cortex reverses the impairing effects of septal GABA receptor activation on spontaneous alternation. Learning & Memory. 7:2000;293-302.
26. Descarries L. The hypothesis of an ambient level of acetylcholine in the central nervous system. Journal of Physiology. 92:1998;215-220.
27. Descarries L., Gisiger V., Steriade M. Diffuse transmission by acetylcholine in the CNS. Progress in Neurobiology. 53:1997;603-625.
28. Diaz del Guante M.A., Carbonell-Hernandez C., Quirarte G., Cruz-Morales S.E., Rivas-Arancibia S., Prado-Alcala R.A. Intrastriatal injection of choline accelerates the acquisition of positively rewarded behaviors. Brain Research Bulletin. 30:1993;671-675.
29. Diaz del Guante M.A., Cruz-Morales S.E., Prado-Alcala R.A. Time-dependent effects of cholinergic blockade of the striatum on memory. Neuroscience Letters. 122:1991;79-82.
30. Disterhoft J.F., Kronforst-Collins M., Oh M.M., Power J.M., Preston A.R., Weiss C. Cholinergic facilitation of trace eyeblink conditioning in aging rabbits. Life Sciences. 64:1999;541-548.
31. Dixon C.E., Bao J., Long D.A., Hayes R.L. Reduced evoked release of acetylcholine in the rodent hippocampus following traumatic brain injury. Pharmacology, Biochemistry and Behavior. 53:1996;679-686.
32. Dornan W.A., McCampbell A.R., Tinkler G.P., Hickman L.J., Bannon A.W., Decker M.W., Gunther K.L. Comparison of site-specific injections into the basal forebrain on water maze and radial arm maze performance in the male rat after immunolesioning with 192 IgG saporin. Behavioural Brain Research. 82:1996;93-101.
33. Durkin T.P. GABAergic mediation of indirect transsynaptic control over basal and spatial memory testing-induced activation of septo-hippocampal cholinergic activity in mice. Behavioural Brain Research. 50:1992;155-165.
34. Durkin T.P., Messier C., de Boer P., Westerink B.H. Raised glucose levels enhance scopolamine-induced acetylcholine overflow from the hippocampus: An in vivo microdialysis study in the rat. Behavioural Brain Research. 49:1992;181-188.
35. Dutar P., Bassant M.H., Senut M.C., Lamour Y. The septohippocampal pathway: Structure and function of a central cholinergic system. Physiological Reviews. 75:1995;393-427.
36. Dykes R.W. Mechanisms controlling neuronal plasticity in somatosensory cortex. Canadian Journal of Physiology and Pharmacology. 75:1997;535-545.
37. Everitt B.J., Robbins T.W. Central cholinergic systems and cognition. Annual Review of Psychology. 48:1997;649-684.
38. Fadda F., Cocco S., Stancampiano R. Hippocampal acetylcholine release correlates with spatial learning performance in freely moving rats. Neuroreport. 11:2000;2265-2269.
39. Fadda F., Melis F., Stancampiano R. Increased hippocampal acetylcholine release during a working memory task. European Journal of Pharmacology. 307:1996;R1-R2.
40. Farr S.A., Flood J.F., Morley J.E. The effect of cholinergic, GABAergic, serotonergic, and glutamatergic receptor modulation on posttrial memory processing in the hippocampus. Neurobiology of Learning and Memory. 73:2000;150-167.
41. Farr S.A., Uezu K., Flood J.F., Morley J.E. Septo-hippocampal drug interactions in post-trial memory processing. Brain Research. 847:1999;221-230.
42. Feig S., Lipton P. Pairing the cholinergic agonist carbachol with patterned Schaffer collateral stimulation initiates protein synthesis in hippocampal CA1 pyramidal cell dendrites via a muscarinic, NMDA-dependent mechanism. Journal of Neuroscience. 13:1993;1010-1021.
43. Ferbinteanu J., McDonald R.J. Dorsal/ventral hippocampus, fornix, and conditioned place preference. Hippocampus. 11:2001;187-200.
44. Funke K., Eysel U.T. Modulatory effects of acetylcholine, serotonin and noradrenaline on the activity of cat perigeniculate neurons. Experimental Brain Research. 95:1993;409-420.
45. Giovannini M.G., Rakovska A., Benton R.S., Pazzagli M., Bianchi L., Pepeu G. Effects of novelty and habituation on acetylcholine, GABA, and glutamate release from the frontal cortex and hippocampus of freely moving rats. Neuroscience. 106:2001;43-53.
46. Givens B., Olton D.S. Cholinergic and GABAergic modulation of medial septal area: Effect on working memory. Behavioral Neuroscience. 104:1990;849-855.
47. Gold P.E. Modulation of emotional and non-emotional memories: Same pharmacological systems, different neuroanatomical systems. McGaugh J.L., Weinberger N.M., Lynch G.S. Brain and memory: Modulation and mediation of neural plasticity. 1995;41-74 Oxford Press, New York.
48. Gold P.E., Hankins L., Edwards R.M., Chester J., McGaugh J.L. Memory interference and facilitation with posttrial amygdala stimulation: Effect on memory varies with footshock level. Brain Research. 86:1975;509-513.
49. Gorman L.K., Pang K., Frick K.M., Givens B., Olton D.S. Acetylcholine release in the hippocampus: Effects of cholinergic and GABAergic compounds in the medial septal area. Neuroscience Letters. 166:1994;199-202.
50. Gu Q. Neuromodulatory transmitter systems in the cortex and their role in cortical plasticity. Neuroscience. 111:2002;43-53.
51. Hagan J.J., Salamone J.D., Simpson J., Iversen S.D., Morris R.G.M. Place navigation in rats is impaired by lesions of medial septum and diagonal band but not nucleus basalis magnocellularis. Behavioural Brain Research. 27:1988;9-20.
52. Hasselmo M.E. Neuromodulation and cortical function: Modeling the physiological basis of behavior. Behavioural Brain Research. 67:1995;1-27.
53. Hasselmo M.E. Neuromodulation: Acetylcholine and memory consolidation. Trends in Cognitive Science. 3:1999;351-359.
54. Hasselmo M.E., Hay J., Ilyn M., Gorchetchnikov A. Neuromodulation, theta rhythm and rat spatial navigation. Neural Networks. 15:2002;689-774.
55. Hironaka N., Tanaka K., Izaki Y., Hori K., Nomura M. Memory-related acetylcholine efflux from rat prefrontal cortex and hippocampus: A microdialysis study. Brain Research. 901:2001;143-150.
56. Inglis F.M., Day J.C., Fibiger H.C. Enhanced acetylcholine release in hippocampus and cortex during the anticipation and consumption of a palatable meal. Neuroscience. 62:1994;1049-1056.
57. Inglis F.M., Fibiger H.C. Increases in hippocampal and frontal cortical acetylcholine release associated with presentation of sensory stimuli. Neuroscience. 66:1995;81-86.
58. Introini-Collison I.B., Dalmaz C., McGaugh J.L. Amygdala beta-noradrenergic influences on memory storage involve cholinergic activation. Neurobiology of Learning and Memory. 65:1996;57-64.
59. Iversen S.D. The pharmacology of memory. Comptes Renus del'Academie des Sciences-Serie III, Sciences de la Vie. 321:1998;209-215.
60. Izquierdo I., da Cunha C., Rosat R., Jerusalinsky D., Ferreira M.B., Medina J.H. Neurotransmitter receptors involved in post-training memory processing by the amygdala, medial septum, and hippocampus of the rat. Behavioral and Neural Biology. 58:1992;16-26.
61. Janis L.S., Glasier M.M., Fulop Z., Stein D.G. Intraseptal injections of 192 IgG saporin produce deficits for strategy selection in spatial-memory tasks. Behavioural Brain Research. 90:1998;23-34.
62. Johnson D.A., Zambon N.J., Gibbs R.B. Selective lesion of cholinergic neurons in the medial septum by 192 IgG-saporin impairs learning in a delayed matching to position T-maze paradigm. Brain Research. 943:2002;132-141.
63. 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.
64. Kesner R.P. Neurobiological views of memory. Martinez J.L., Kesner R.P. Neurobiology of learning and memory. 1998;361-416 Academic Press, San Diego.
65. Kilgard M.P., Merzenich M.M. Cortical map reorganization enabled by nucleus basalis activity. Science. 279:1998;1714-1718.
66. Kilgard M.P., Merzenich M.M. Order-sensitivity plasticity in adult primary auditory cortex. Proceedings of the National Academy of Sciences of the United States of America. 99:2002;3205-3209.
67. Kim J.J., Lee H.J., Han J.S., Packard M.G. Amygdala is critical for stress-induced modulation of hippocampal long-term potentiation and learning. Journal of Neuroscience. 21:2001;5222-5228.
68. Kirkwood A., Rozas C., Kirkwood J., Perez F., Bear M.F. Modulation of long-term synaptic depression in visual cortex by acetylcholine and norepinephrine. Journal of Neuroscience. 19:1999;1599-1609.
69. Kobayashi T., Iwasaki T. Functional dissociation of striatal and hippocampal cholinergic systems in egocentric and allocentric localization: Effect of overtraining. Nihon Shinkei Seishin Yakurigaku Zasshi. 20:2000;113-121.
70. Kopf S.R., Buchholzer M.L., Hilgert M., Loffelholz K., Klein J. Glucose plus choline improve passive avoidance behaviour and increase hippocampal acetylcholine release in mice. Neuroscience. 103:2001;365-371.
71. 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.
72. Krech D., Rosenzweig M.R., Bennett E.L., Krueckel B. Enzyme concentrations in the brain and adjustive behavior-patterns. Science. 120:1954;994-996.
73. Krugel U., Bigl V., Eschrich K., Bigl M. Deafferentation of the septo-hippocampal pathway in rats as a model of the metabolic events in Alzheimer's disease. International Journal of Developmental Neuroscience. 19:2001;263-277.
74. LeBlanc C.J., Deacon T.W., Whatley B.R., Dinsmore J., Lin L., Isacson O. Morris water maze analysis of 192-IgG-saporin-lesioned rats and porcine cholinergic transplants to the hippocampus. Cell Transplantation. 8:1999;131-142.
75. Lamprea M.R., Cardenas F.P., Silveira R., Morato S., Walsh T.J. Dissociation of memory and anxiety in a repeated elevated plus maze paradigm: Forebrain cholinergic mechanisms. Behavioural Brain Research. 117:2000;97-105.
76. Lapchak P.A., Jenden D.J., Hefti F. Compensatory elevation of acetylcholine synthesis in vivo by cholinergic neurons surviving partial lesions of the septohippocampal pathway. Journal of Neuroscience. 11:1991;2821-2828.
77. Leanza G., Nilsson O.G., Björklund A. Compensatory changes of in vivo acetylcholine and noradrenaline release in the hippocampus after partial deafferentation, as monitored by microdialysis. Brain Research. 615:1993;147-159.
78. Leanza G., Nilsson O.G., Wiley R.G., Björklund A. Selective lesioning of the basal forebrain cholinergic system by intraventricular 192IgG-Saporin: Behavioral, biochemical and stereological studies in the rat. European Journal of Neuroscience. 7:1995;329-343.
79. Lehmann O., Jeltsch H., Lazarus C., Tritschler L., Bertrand F., Cassel J.C. Combined 192 IgG-saporin and 5,7-dihydroxytryptamine lesions in the male rat brain: A neurochemical and behavioral study. Pharmacology Biochemistry and Behavior. 72:2002;899-912.
80. Li B., Duysen E.G., Volpicelli-Daley L.A., Levey A.I., Lockridge O. Regulation of muscarinic acetylcholine receptor function in acetylcholinesterase knockout mice. Pharmacology, Biochemistry and Behavior. 74:2003;977-986.
81. Lilliquist M.W., Burkhalter E.C., Lobaugh N.J., Amsel A. Age-dependent effects of hippocampal muscarinic receptor blockade on memory-based learning in the developing rat. Behavioural Brain Research. 53:1993;119-125.
82. Linster C., Maloney M., Patil M., Hasselmo M.E. Enhanced cholinergic suppression of previously strengthened synapses enables the formation of self-organized representations in olfactory cortex. Neurobiology of Learning and Memory. 80:2003;302-314.
83. Liu Y., Jia W., Gu Q., Cynader M. Involvement of muscarinic acetylcholine receptors in regulation of kitten visual cortex plasticity. Developmental Brain Research. 79:1994;63-71.
84. Maelicke A., Schrattenholz A., Samochocki M., Radina M., Albuquerque E.X. Allosterically potentiating ligands of nicotinic receptors as a treatment strategy for Alzheimer's disease. Behavioural Brain Research. 113:2000;199-206.
85. Marder E., Thirumalai V. Cellular, synaptic and network effects of neuromodulation. Neural Networks. 15:2002;479-493.
86. Mark G.P., Weinberg J.B., Rada P.V., Hoebel B.G. Extracellular acetylcholine is increased in the nucleus accumbens following the presentation of an aversively conditioned taste stimulus. Brain Research. 688:1995;184-188.
87. Markowska A.L., Olton D.S., Givens B. Cholinergic manipulations in the medial septal area: Age-related effects on working memory and hippocampal electrophysiology. Journal of Neuroscience. 15:1995;2063-2073.
88. Matthews D.B., Best P.J. Fimbria/fornix lesions facilitate the learning of a nonspatial response task. Psychonomic Bulletin & Review. 2:1995;113-116.
89. McDonald R.J., White N.M. A triple dissociation of memory systems: Hippocampus, amygdala, and dorsal striatum. Behavioral Neuroscience. 107:1993;3-22.
90. McDonald R.J., White N.M. Parallel information processing in the water maze: Evidence for independent memory systems involving dorsal striatum and hippocampus. Behavioral and Neural Biology. 61:1994;260-270.
91. 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.
92. McEwen B.S. Plasticity of the hippocampus: Adaptation to chronic stress and allostatic load. Annals of the New York Academy of Sciences. 933:2001;265-277.
93. McGaugh J.L. Memory consolidation and the amygdala: A systems perspective. Trends in Neurosciences. 25:2002;456.
94. McGaugh J.L., Gold P.E. Modulation of memory processes with electrical stimulation of the brain. Rosenzweig M., Bennett E. Neural mechanisms of learning and memory. 1976;549-560 The MIT Press, Cambridge, MA.
95. McIntyre C.K., Marriott L.K., Gold P.E. Cooperation between memory systems: Acetylcholine release in the amygdala correlates positively with good performance on a hippocampus-dependent task. Behavioral Neuroscience. 117:2003;320-326.
96. McIntyre C.K., Marriott L.K., Gold P.E. Patterns of brain acetylcholine release predict individual differences in preferred learning strategies in rats. Neurobiology of Learning and Memory. 79:2003;177-183.
97. 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.
98. McIntyre C.K., Power A.E., Roozendaal B., McGaugh J.L. Role of the basolateral amygdala in memory consolidation. Annals of the New York Academy of Sciences. 985:2003;273-293.
99. McIntyre C.K., Ragozzino M.E., Williams L., Gold P.E. Intra-amygdala infusions of scopolamine impair performance on a conditioned place preference task but not a win-shift task. Behavioural Brain Research. 95:1998;219-226.
100. McMahon R.W., Sobel T.J., Baxter M.G. Selective immunolesions of hippocampal cholinergic input fail to impair spatial working memory. Hippocampus. 7:1997;130-136.
101. McNamara R.K., Skeleton R.W. The neuropharmacological and neurochemical basis of place learning in the Morris water maze. Brain Research Reviews. 18:1993;33-49.
102. McNamara R.K., Skeleton R.W. Effects of intracranial infusions of chlordiazepoxide on spatial learning in the Morris water maze. I. Neuroanatomical specificity. Behavioural Brain Research. 59:1993;175-191.
103. McNay E.C., Gold P.E. 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. 18:1998;3853-3858.
104. Messier C., Durkin T., Mrabet O., Destrade C. Memory-improving action of glucose: Indirect evidence for a facilitation of hippocampal acetylcholine synthesis. Behavioural Brain Research. 39:1990;135-143.
105. Mesulam M.M., Guillozet A., Shaw P., Levey A., Duysen E.G., Lockridge O. Acetylcholinesterase knockouts establish central cholinergic pathways and can use butyrylcholinesterase to hydrolyze acetylcholine. Neuroscience. 110:2002;627-639.
106. Meyer J.J., Allen D.D., Yokel R.A. Hippocampal acetylcholine increases during eyeblink conditioning in the rabbit. Physiology and Behavior. 60:1996;1199-1203.
107. Miranda M.I., Ramirez-Lugo L., Bermudez-Rattoni F. Cortical cholinergic activity is related to the novelty of the stimulus. Brain Research. 882:2000;230-235.
108. Mizumori S.J., Cooper B.G., Leutgeb S., Pratt W.E. A neural systems analysis of adaptive navigation. Molecular Neurobiology. 21:2000;57-82.
109. Myhrer T. Neurotransmitter systems involved in learning and memory in the rat: A meta-analysis based on studies of four behavioral tasks. Brain Research Reviews. 41:2003;268-287.
110. Nagle, R. A., Liberatore, M. A., Zombon, N. J., Pokala, V. N., Li, P. K., Pokala, V. N., & Johnson, D.A. (2002). Effect of selective cholinergic lesioning of basal forebrain with 192IgG-saporin on neurotransmitter concentrations in the hippocampus of rat. In Society for Neuroscience, 32nd Annual Meeting, Orlando.
111. Nilsson O.G., Leanza G., Rosenblad C., Lappi D.A., Wiley R.G., Bjöklund A. Spatial learning impairments in rats with selective immunolesion of the forebrain cholinergic system. Neuroreport. 3:1992;1005-1008.
112. Nistri A., Di Angelantonio S. Enhancement of neuronal nicotinic receptor activity of rat chromaffin cells by a novel class of peptides. Annals of the New York Academy of Sciences. 971:2002;100-107.
113. Ogren S.O., Kehr J., Schott P.A. Effects of ventral hippocampal galanin on spatial learning and on in vivo acetylcholine release in the rat. Neuroscience. 75:1996;1127-1140.
114. Ohno M., Yamamoto T., Watanabe S. Blockade of hippocampal M1 muscarinic receptors impairs working memory performance of rats. Brain Research. 650:1994;260-266.
115. Olariu A., Tran M.H., Yamada K., Mizuno M., Hefco V., Nabeshima T. Memory deficits and increased emotionality induced by beta-amyloid (25-35) are correlated with the reduced acetylcholine release and altered phorbol dibutyrate binding in the hippocampus. Journal of Neural Transmission, General Section. 108:2001;1065-1079.
116. Olton D.S. Experimental strategies to identify the neurobiological bases of memory: Lesions. Martinez J.L. Jr., Kesner R.P. Learning and memory: A biological view. 2nd ed. 1991;441-466.
117. Orsetti M., Casamenti F., Pepeu G. Enhanced acetylcholine release in the hippocampus and cortex during acquisition of an operant behavior. Brain Research. 724:1996;89-96.
118. Packard M.G., Hirsch R., White N.M. Differential effects of fornix and caudate nucleus lesions on two radial maze tasks: Evidence for multiple memory systems. Journal of Neuroscience. 9:1989;1465-1472.
119. 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.
120. Pang K.C.H., Nocera R., Secor A.J., Yoder R.M. GABAergic septohippocampal neurons are not necessary for spatial memory. Hippocampus. 11:2001;814-827.
121. Parent M.B., Laurey P.T., Wilkniss S., Gold P.E. Intraseptal infusions of muscimol impair spontaneous alternation performance: Infusions of glucose into the hippocampus, but not the medial septum, reverse the deficit. Neurobiology of Learning and Memory. 68:1997;75-85.
122. Perry T., Hodges H., Gray J. Behavioral, histological and immunocytochemical consequences following 192 IgG-saporin immunolesions of the basal forebrain cholinergic system. Brain Research Bulletin. 54:2001;29-48.
123. Pokala, V. N., Libertore, M. A., Zambon, N. J., Nagle, R. A., Li, P. K., Witt-Enderby, P. A., & Johnson, D. A. (2002). Effect of 192 IgG-saporin medial septum lesion on hippocampal receptor density in rats. In Society for Neuroscience, 32nd Annual Meeting, Orlando.
124. Poldrack R.A., Packard M.G. Competition among multiple memory systems: Converging evidence from animal and human brain studies. Neuropsychologia. 41:2003;245-251.
125. Poucet B., Buhot M.C. Effects of medial septal or unilateral hippocampal inactivations on reference and working spatial memory in rats. Hippocampus. 4:1994;315-321.
126. Power A.E., McIntyre C.K., Litmanovich A., McGaugh J.L. Cholinergic modulation of memory in the basolateral amygdala involves activation of both m1 and m2 receptors. Behavioural Pharmacology. 14:2003;207-213.
127. Power A.E., Roozendaal B., McGaugh J.L. Glucocorticoid enhancement of memory consolidation in the rat is blocked by muscarinic receptor antagonism in the basolateral amygdala. European Journal of Neuroscience. 12:2000;3481-3487.
128. Power A.E., Vazdarjanova A., McGaugh J.L. Muscarinic cholinergic influences in memory consolidation. Neurobiology of Learning and Memory. 80:2003;178-193.
129. Power J.M., Oh M.M., Disterhoft J.F. Metrifonate decreases sIAHP in CA1 pyramidal neurons in vitro. Journal of Neurophysiology. 85:2001;319-322.
130. Ragozzino M.E., Gold P.E. Glucose injections into the medial septum reverse the effects of intraseptal morphine infusions on hippocampal acetylcholine output and memory. Neuroscience. 68:1995;981-988.
131. 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.
132. Ragozzino M.E., Parker M.E., Gold P.E. Spontaneous alternation and inhibitory avoidance impairments with morphine injections into the medial septum: Attenuation by glucose administration. Brain Research. 597:1992;241-249.
133. 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. 93:1996;4693-4698.
134. Ragozzino M.E., Wenk G.L., Gold P.E. Glucose attenuates morphine-induced decrease in hippocampal acetylcholine output: An in vivo microdialysis study in rats. Brain Research. 655:1994;77-82.
135. Ragozzino M.E. Acetylcholine actions in the dorsomedial striatum support the flexible shifting of response patterns. Neurobiology of Learning and Memory. 80:2003;257-267.
136. Rasmusson D.D. The role of acetylcholine in cortical synaptic plasticity. Behavioural Brain Research. 115:2000;205-218.
137. Restle F. Discrimination of cues in mazes: A resolution of the place-vs.-response question. Psychological Review. 64:1957;217-228.
138. Riekkinen P.J., Sirviö J., Riekkinen P. Relationship between the cortical choline acetyltransferase content and EEG delta-power. Neuroscience Research. 8:1990;12-20.
139. Riekkinen P. Jr., Schmidt B., Riekkinen M. Behavioral characterization of metrifonate-improved acquisition of spatial information in medial septum-lesioned rats. European Journal of Pharmacology. 323:1997;11-96.
140. Roozendaal B., McGaugh J.L. Glucocorticoid receptor agonist and antagonist administration into the basolateral but not central amygdala modulates memory storage. Neurobiology of Learning and Memory. 67:1997;176-179.
141. Roozendaal B., Nguyen B.T., Power A.E., McGaugh J.L. Basolateral amygdala noradrenergic influence enables enhancement of memory consolidation induced by hippocampal glucocorticoid receptor activation. Proceedings of the National Academy of Sciences of the United States of America. 96:1999;11642-11647.
142. Sarter M., Bruno J.P. Cognitive functions of cortical acetylcholine: Toward a unifying hypothesis. Brain Research Reviews. 23:1997;28-46.
143. Sarter M., Bruno J.P. Cortical cholinergic inputs mediating arousal, attentional processing and dreaming: Differential afferent regulation of the basal forebrain by telencephalic and brainstem afferents. Neuroscience. 95:2000;933-952.
144. Sarter M., Bruno J.P. The neglected constituent of the basal forebrain corticopetal projection system: GABAergic projections. European Journal of Neuroscience. 15:2002;1867-1873.
145. Sarter M., Bruno J.P., Turchi J. Basal forebrain afferent projections modulating cortical acetylcholine, attention and implications for neuropsychiatric disorders. Annals of the New York Academy of Sciences. 877:1999;368-382.
146. Savage, L. M., Chang, Q., & Gold, P. E. (2003). Diencephalic damage decreases hippocampal acetylcholine release during spontaneous alternation testing. Learning & Memory. in press.
147. Schroeder J., Wingard J.C., Packard M.G. Post-training reversible inactivation of hippocampus reveals interference between memory systems. Hippocampus. 12:2002;280-284.
148. Segal M., Auerbach J.M. Muscarinic receptors involved in hippocampal plasticity. Life Sciences. 60:1997;1085-1091.
149. Schafe G.E., Nader K., Blair H.T., LeDoux J.E. Memory consolidation of Pavlovian fear conditioning: A cellular and molecular perspective. Trends in Neurosciences. 24:2001;540-546.
150. Shinjo H., Ueki A., Miwa C., Morita Y. Effect of entorhinal cortex lesion on hippocampal cholinergic system in rat in operant learning task as studied by in vivo brain microdialysis. Journal of the Neurological Sciences. 157:1998;13-18.
151. Shors T.J. Acute stress rapidly and persistently enhances memory formation in the male rat. Neurobiology of Learning and Memory. 75:2001;10-29.
152. Stackman R.W., Walsh T.J. Chlorodiazepoxide-induced working memory impairments: Site specificity and reversal by flumazenil, (RO15-1788). Behavioral and Neural Biology. 57:1992;233-243.
153. Tang Y., Aigner T.G. Release of cerebral acetylcholine increases during visually mediated behavior in monkeys. Neuroreport. 7:1996;2231-2235.
154. Tang A.C., Bartels A.M., Sejnowski T.J. Effects of cholinergic modulation on responses of neocortical neurons to fluctuating input. Cerebral Cortex. 7:1997;502-509.
155. Tolman E.C., Ritchie B.F., Kalish D. Studies in spatial learning: II. Place learning versus response. Journal of Experimental Psychololgy. 36:1946;221-229.
156. van der Zee E.A., Luiten P.G. Muscarinic acetylcholine receptors in the hippocampus, neocortex and amygdala: A review of immunocytochemical localization in relation to learning and memory. Progress in Neurobiology. 58:1999;409-471.
157. Vizi E.S., Kiss J.P. Neurochemistry and pharmacology of the major hippocampal transmitter systems: Synaptic and nonsynaptic interactions. Hippocampus. 8:1998;566-607.
158. Wallenstein G.V., Vago D.R. Intrahippocampal scopolamine impairs both acquisition and consolidation of contextual fear conditioning. Neurobiology of Learning and Memory. 75:2001;245-252.
159. Warburton E.C., Koder T., Cho K., Massey P.V., Duguid G., Barker G.R.I., Aggleton J.P., Bashir Z.I., Brown M.W. Cholinergic neurotransmission is essential for perirhinal cortical plasticity and recognition memory. Neuron. 38:2003;987-996.
160. Walsh T.J., Gandhi C., Stackman R.W. Reversible inactivation of the medial septum or nucleus basalis impairs working memory in rats: A dissociation of memory and performance. Behavioral Neuroscience. 112:1998;1114-1124.
161. Walsh T.J., Herzog C.D., Ghandi C., Stackman R.W., Wiley R.G. Injection of IgG 192-saporin into the medial septum produces cholinergic hypofunction and dose-dependent working memory deficits. Brain Research. 726:1996;69-79.
162. Weimann J.M., Marder E. Switching neurons are integral members of multiple oscillatory networks. Current Biology. 4:1994;896-902.
163. Weinberger N.M. Physiological memory in the primary auditory cortex: Characteristics and mechanisms. Neurobiology of Learning and Memory. 70:1998;226-251.
164. Weinberger N.M. Memory codes: New concept for old problem. Gold P.E., Greenough W.T. Memory consolidation: Essays in Honor of James L. McGaugh - A Time to Remember. 2001;321-342 American Psychological Association, Washington, DC.
165. Weinberger N.M. The nucleus basalis and memory codes: Auditory cortical plasticity and the induction of specific, associative behavioral memory. Neurobiology of Learning and Memory. 80:2003;268-284.
166. 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.
167. Whitehouse P.J., Price D.L., Struble R.G., Clark A.W., Coyle J.T., Delon M.R. Alzheimer's disease and senile dementia: Loss of neurons in the basal forebrain. Science. 215:1982;1237-1239.
168. Wiley R.G. Neural lesioning with ribosome-inactivating proteins: Suicide transport and immunolesioning. Trends in Neuroscience. 15:1992;285-290.
169. Winkler J., Thal L.J., Gage F.H., Fisher L.J. Cholinergic strategies for Alzheimer's disease. Journal of Molecular Medicine. 76:1998;555-567.
170. Woolf N.J. The critical role of cholinergic basal forebrain neurons in morphological change and memory encoding: A hypothesis. Neurobiology of Learning and Memory. 66:1996;258-266.
171. Woolf N.J. A structural basis for memory storage in mammals. Progress in Neurobiology. 55:1998;59-77.
172. Wrenn C.C., Lappi D.A., Wiley R.G. Threshold relationship between lesion extent of the cholinergic basal forebrain in the rat and working memory impairment in the radial maze. Brain Research. 847:1999;284-298.
173. Wu M., Shanabrough M., Leranth C., Alreja M. Cholinergic excitation of septohippocampal GABA but not cholinergic neurons: Implications for learning and memory. Journal of Neuroscience. 20:2000;3900-3908.
174. Yamamuro Y., Hori K., Tanaka J., Iwano H., Nomura M. Septo-hippocampal cholinergic system under the discrimination learning task in the rat: A microdialysis study with the dual-probe approach. Brain Research. 684:1995;1-7.
175. Yamamuro Y., Iwano H., Sensui N., Hori K., Nomura M. Acetylcholine in the hippocampus during the discrimination learning performance in a rat model of chronic cerebral ischaemia. Neuroreport. 7:1996;1837-1840.
176. Yeshenko, O. V., & Mizumori, S. J. Y. (2002). Differential firing of medial dorsal striatum neurons during place and response strategy use on a t-maze. In Society for Neuroscience, 32nd Annual Meeting, Orlando.
177. Zigmond M.J., Abercrombie E.D., Stricker E.M. Partial damage to nigrostriatal bundle: Compensatory changes and the action of L-DOPA. Journal of Neural Transmission, Supplementum. 29:1990;217-232.