Modulation of cognitive processes by transsynaptic activation of the basal forebrain

Behavioural Brain Research

Volumn 84, Issue 1-2, 1997, Pages 1-22

  Givens, Ben ^a   Sarter, Martin ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

basal forebrain; behavioral consequences; neurobiological consequences; transsynaptic activation

Indexed keywords

NEUROTRANSMITTER;

ANIMAL EXPERIMENT; BEHAVIOR; BRAIN INJURY; COGNITION; FOREBRAIN; HUMAN; HUMAN EXPERIMENT; NONHUMAN; PRIORITY JOURNAL; REVIEW;

EID: 0031052003     PISSN: 01664328     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0166-4328(96)00146-5     Document Type: Article

References (217)

1. Adolphs, R., Tranel, D., Damasio, H. and Damasio, A.R., Fear and the human amygdala, J. Neurosci., 15 (1995) 5879-5891.
2. Allen, C.N. and Crawford, I.L., GABAergic agents in the medial septal nucleus affect hippocampal theta rhythm and acetylcholine utilization, Brain Res., 322 (1984) 261-267.
3. Alonso, A., Faure, M.-P. and Beaudet, A., Neurotensin promotes oscillatory bursting behavior and is internalized in basal forebrain cholinergic neurons, J. Neurosci., 14 (1994) 5778-5792.
4. Aston-Jones, G., Rajkowski, J., Kubiak, P. and Alexinsky, T., Locus coeruleus neurons in monkey are selectively activated by attended cues in a vigilance task, J. Neurosci., 14 (1994) 4467-4480.
5. Beatty, W.W., Butters, N. and Janowski, D.S., Patterns of memory failure after scopolamine treatment: implications for cholinergic hypothesis of dementia, Behav. Neural Biol., 45 (1986) 196-211.
6. Bechara, A., Tranel, D., Damasio, H., Adolphs, R., Rockland, C. and Damasio, A.R., Double dissociation of conditioning and declarative knowledge relative to the amygdala and hippocampus in humans, Science, 269 (1995) 1115-1118.
7. Beninger, R.J., Ingles, J.L., Mackenzie, P.J., Jhamandas, K. and Boegman, R.J., Muscimol injections into the nucleus basalis magnocellularis of rats: selective impairment of working memory in the double Y-maze, Brain Res., 597 (1992) 66-73.
8. Bialowas, J. and Frotscher, M., Choline acetyltransferase-immunoreactivity neurons and terminals in the rat septal complex: A combined light and electron microscope study, J. Comp. Neural., 259 (1987) 298-307.
9. Blaker, W.D., Cheney, D.L. and Costa, E., GABA-A vs. GABA-B modulation of septal-hippocampal interconnections. In I. Hanin (Ed.), Dynamics of Cholinergic Function, Plenum Press, New York, 1986, pp. 953-961.
10. Blaker, W.D., Peruzzi, G. and Costa, E., Behavioral and neurochemical differentiation of specific projections in the septal-hippocampal cholinergic pathway in the rat. Proc. Nat. Acad. Sci. USA, 81 (1984) 1880-1882.
11. Boegman, R.J., Cockhill, J., Jhamandas, K. and Beninger, R.J., Excitotoxic lesions of rat basal forebrain: Differential effects on choline acetyltransferase in the cortex and amygdala, Neuroscience, 51 (1992) 129-135.
12. Boix, F., Sandor, P., Nogueira, P.J., Huston, J.P. and Schwarting, R.K., Relationship between dopamine release in nucleus accumbens and place preference induced by substance P injected into the nucleus basalis magnocellularis region, Neuroscience, 64 (1995) 1045-1055.
13. Bostock, E., Gallagher, M. and King, R.A., Effects of opioid microinjections into the medial sepal area on spatial memory in rats, Behav. Neurosci., 102 (1988) 643-652.
14. Brioni, J.D., Decker, M.W., Gamboa, L.P., Izquierdo, I. and McGaugh, J.L., Muscimol injections in the medial septum impair spatial learning, Brain Res., 522 (1990) 227-234.
15. Buzsaki, G., Bickford, R.G., Ponomareff, G., Thal, L.J., Mandel, R. and Gage, F.H., Nucleus basalis and thalamic control of neocortical activity in the freely moving rat. J. Neurosci., 8 (1988) 4007-4026.
16. Casamenti, F., Deffenu, G., Abbamondi, A.L. and Pepeu, G., Changes in cortical acetylcholine output induced by modulation of the nucleus basalis, Brain Res. Bull., 16 (1986) 689-695.
17. Cassel, J.C. and Jeltsch, H., Serotonergic modulation of cholinergic function in the central nervous system: Cognitive implications, Neuroscience, 69 (1995) 1-41.
18. Chan-Palay, V., Galanin hyperinnervates surviving neurons of the human basal nucleus of Meynert in dementias of Alzheimer's and Parkinson's disease: a hypothesis for the role of galanin in accentuating cholinergic dysfunction in dementia, J. Comp. Neural., 273 (1988) 543-557.
19. Chiba, A.A., Bucci, D.J., Holland, P.C. and Gallagher, M., Basal forebrain cholinergic lesions disrupt increments but not decrements in conditioned stimulus processing, J. Neurosci., 15 (1995) 7315-7322.
20. Chrobak, J.J. and Napier, T.C., Intraseptal administration of bicuculline produce working memory impairments in the rat, Behav. Neural Biol., 55 (1991) 247-254.
21. Chrobak, J.J. and Napier, T.C., Antagonism of GABAergic transmission within the septum disrupts working/episodic memory in the rat, Neuroscience, 47 (1992) 833-841.
22. Chrobak, J.J., Stackman, R.W. and Walsh, T.J., Intraseptal administration of muscimol produces dose-dependent memory impairments in the rat, Behav. Neural Biol., 52 (1989) 357-369.
23. Chu, D.C.M., Albin, R.L., Young, A.B. and Penney, J.B., Distribution and kinetics of GABA-B binding sites in rat central nervous system: A quantitative autoradiographic study, Neuroscience, 34 (1990) 341-357.
24. Churchhill, L. and Kalivas, P.W., A topographically organized gamma-aminobutyric acid projection from the ventral pallidum to the nucleus accumbens in the rat, J. Comp. Neurol., 345 (1994) 579-595.
25. Clement, J.D., Transmitter timecourse in the synaptic cleft: its role in central synaptic function, Trends Neurosci., 19 (1996) 163-171.
26. Cole, A.E. and Nicoll, R.A., Characterization of a slow cholinergic post-synaptic potential recorded in vitro from rat hippocampal pyramidal cells, J. Neurophysiol., 352 (1984) 173-188.
27. Collerton, D., Cholinergic function and intellectual decline in Alzheimer's disease, Neuroscience, 19 (1986) 1-28.
28. Costa, E., Panula, P., Thompson, H.K. and Cheney, D.L., The transsynaptic regulation of the septal-hippocampal cholinergic neurons, Life Sci., 32 (1983) 165-179.
29. Cuello, A.C., Priestley, J.V. and Paxinos, G., Substance P and enkephalin containing pathways. In G. Paxinos (Ed.) The Rat Nervous System, Academic Press, Australia, 1985, pp. 441-469.
30. Cui, Y., Lee, T.F. and Wang, L.C.H., Thermoregulatory responses following injection of 5-hydroxytryptamine into the septohippocampal complex in rats, Pharmacol. Biochem. Behav., 45 (1993) 935-939.
31. Day, J.C. and Fibiger, H.C., Dopaminergic regulation of cortical acetylcholine release, Synapse, 12 (1992) 281-286.
32. Day, J.C. and Fibiger, H.C., Dopaminergic regulation of cortical acetylcholine release: effects of dopamine receptor agonists, Neuroscience, 54 (1993) 643-648.
33. Day, J.C. and Fibiger, H.C., Dopaminergic regulation of septohippocampal cholinergic neurons, J. Neurochem., 63 (1994) 2086-2092.
34. Decker, M.W. and McGaugh, J.L., The role of interactions between the cholinergic system and other neuromodulatory systems in learning and memory, Synapse, 7 (1991) 151-168.
35. Dekker, A.J., Conner, D.J. and Thal, L.J., The role of cholinergic projections from the nucleus basalis in memory, Neurosci. Biobehav. Rev., 15 (1991) 299-317.
36. DeKosky, S.T., Harbaugh, R.E., Schmitt, F.A., Bakay, R.A., Chui, H.C., Knopman, D.S., Reeder, T.M., Shelter, A.G., Senter, H.J. and Markesbery, W.R., Cortical biopsy in Alzheimer's disease: Diagnostic accuracy and neurochemical, neuropathological, and cognitive correlations, Ann. Neural., 32 (1992) 625-632.
37. B receptors in the basal forebrain selectively impairs working memory of rats in the double Y-maze, Brain Res., 641 (1994) 29-38.
38. Dickinson-Anson, H. and McGaugh, J.L., Infusion of the GABAergic antagonist bicuculline into the medial septal area does not block the impairing effects of systemically administered midazolam on inhibitory avoidance retention, Behav. Neural Biol., 62 (1994) 253-258.
39. Drugan, R.C., Skolnick, P., Paul, S.M. and Crawley, J.N., Low doses of muscimol produce anticonflict actions in the lateral septum of the rat, Neuropharmacology, 26 (1986) 203-205.
40. Dudchenko, P. and Sarter, M., GABAergic control of basal forebrain cholinergic neurons and memory. Behav. Brain Res., 42 (1991) 33-41.
41. Dudchenko, P. and Sarter, M., Failure of a chlordiazepoxide to reproduce the behavioral effects of muscimol administered into the basal forebrain, Behav. Brain Res., 47 (1992) 202-205.
42. Dunnett, S.B., Comparative effects of cholinergic drugs and nucleus basalis or flmbria-fornix lesions on delayed matching to sample in rats. Psychopharmacology, 87 (1985) 357-363.
43. Dunnett, S.B., Everitt, B.J. and Robbins, T.W., The basal forebrain-cortical cholinergic system: Interpreting the functional consequences of excitotoxic lesions, Trends Neurosci., 14 (1991) 494-501.
44. Dunnett, S.B., Wareham, A.T. and Torres, E.M., Cholinergic blockade of prefrontal cortex and hippocampus disrupts short-term memory in rats, NeuroReport, 1 (1990) 61-64.
45. Durkin, T.P., GABAergic mediation of indirect transsynaptic control over basal and spatial memory testing-induced activation of septo-hippocampal cholinergic activity in mice, Behav. Brain Res., 50 (1992) 155-165.
46. Durkin, T.P., Spatial working memory over long retention intervals: Dependence on sustained cholinergic activation in the septohippocampal or nucleus basalis magnocellularis-cortical pathways, Neuroscience, 62 (1994) 681-693.
47. Durkin, T.P., Galey, D., Micheau, J., Beslon, H. and Jaffard, R., The effects of acute intraseptal injection of haloperidol in vivo on hippocampal cholinergic function in the mouse, Brain Res., 376 (1986) 420-424.
48. Durkin, T.P. and Toumane, A., Septo-hippocampal and nBM-cortical cholinergic neurones exhibit differential time-courses of activation as a function of both type and duration of spatial memory testing in mice, Behav. Brain Res., 50 (1992) 43-52.
49. Dutar, P., Bassant, M.-H., Senut, M.-C. and Lamour, Y., The septohippocampal pathway: Structure and function of a central cholinergic system, Physiol. Rev., 75 (1995) 393-412.
50. Dutar, P., Rascol, O., Jobert, A. and Lamour, Y., Comparison of septo-hippocampal with basalo-cortical projection neurons in the rat: an electrophysiological approach, Neurosci. Lett., 63 (1986) 86-90.
51. Eichenbaum, H., Otto, T. and Cohen, N.J., Two functional com-ponents of the hippocampal memory system, Behav. Brain Sci., 17 (1994) 449-518.
52. Engelmann, M., Bures, J. and Landgraf, R., Vasopressin administration via microdialysis into the septum interferes with the acquisition of spatial memory in rats, Neuosci. Lett., 142 (1992) 69-72.
53. Engelmann, M. and Landgraf, R., Microdialysis administration of vasopressin into the septum improves social recognition in Brattleboro rats, Physiol. Behav., 55 (1994) 145-149.
54. Fibiger, H.C., Cholinergic mechanisms in learning, memory and dementia: review of recent evidence, Trends Neurosci., 14 (1991) 220-223.
55. Fisone, G., Wu, C.F., Consolo, S., Nordstrom, O., Brynne, N., Bartfai, R., Melander, T. and Hökfelt, T., Galanin inhibits acetylcholine release in the ventral hippocampus of the rat: histochemical, autoradiographic, in vivo, and in vitro studies, Proc. Natl. Acad. Sci. USA, 84 (1987) 7339-7343.
56. Freund, T.F. and Antal, M., GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus. Nature, 336 (1988) 170-173.
57. Freund, T.F. and Meskenaite, V., Gamma-aminobutyric acid-containing basal forebrain neurons innervate inhibitory interneurons in the neocortex, Proc. Nat. Acad. Sci. USA, 89 (1992) 738-742.
58. Fried, P.A., Septum and behavior: A review, Psychol. Bull., 78 (1972) 292-310.
59. Gall, C. and Moore, R.Y., Distribution of enkephalin, substance P, tyrosine hydroxylase, and 5-hydroxytryptamine immunoreactivity in the septal region of the rat, J. Comp. Neural., 225 (1984) 212-227.
60. Gallagher, J.P., Zheng, F., Hasuo, H. and Shinnick-Gallagher, P., Activities of neurons within the rat dorsolateral septal nucleus (DLSN), Prog. Neurobiol, 45 (1995) 373-395.
61. Gallagher, M., Meagher, M.W. and Bostock, E., Effects of opiate manipulations on latent inhibition in rabbits: Sensitivity of the medial septal region to intracranial treatments, Behav. Neurosci., 101 (1987) 315-324.
62. Gao, B., Hornung, J.P. and Fritschy, J.M., Identification of distinct GABAA-receptor subtypes in cholinergic and parval-bumin-positive neurons of the rat and marmoset medial septumdiagonal band complex, Neuroscience, 65 (1995) 101-117.
63. Gaykema, G.P.A., Van der Kuil, J., Hersh, L.B. and Luiten, P.G.M., Patterns of direct projections from the hippocampus to the medial septum-diagonal band complex: anterograde tracing with phasoleus vulgaris leucoagglutinin combined with immunochemistry of choline acetyltransferase, Neuroscience, 43 (1991) 349-360.
64. Gaykema, G.P.A. and Zaborszky, L., Direct catecholaminergic-cholinergic interactions in the basal forebrain. II. Substantia nigra-ventral tegmental area projections to basal forebrain cholinergic neurons, J. Comp. Neural (in press) (1996)
65. Gaykema, R.P., van Weeghel, R., Hersh, L.B. and Luiten, P.G., Prefrontal cortical projections to the cholinergic neurons in the basal forebrain, J. Comp. Neural., 303 (1991) 563-583.
66. Giovannini, M.G., Mutolo, D., Bianchi, L., Michelassi, A. and Pepeu, G., NMDA receptor antagonists decrease GABA outflow from the septum and increase acetylcholine outflow from the hippocampus: A microdialysis study, J. Neurosci., 14 (1994) 1358-1365.
67. Givens, B., Behavioral correlates of single units in the medial septal area: The effect of ethanol, Neuroscience, 71 (1996) 417-427.
68. Givens, B. and Breese, G.R., Electrophysiological evidence that ethanol alters function of medial septal area without affecting lateral septal function, J. Pharmacol. Exp. Ther., 253 (1990) 95-103.
69. Givens, B. and Olton, D., Working memory and cholinergic autoregulation in the medial septal area. In E.D. Levin, M.W. Decker and L.L. Butcher (Eds.) Neurotransmitter interactions and cognitive function. Birkhauser, Boston, 1992, pp. 301-311.
70. Givens, B. and Olton, D.S., Cholinergic and GABAergic modulation of medial septal area: Effect on working memory, Behav. Neurosci., 104 (1990) 849-855.
71. Givens, B. and Olton, D.S., Local modulation of basal forebrain: Effects on working and reference memory, J. Neurosci., 14 (1994) 3578-3587.
72. Givens, B. and Olton, D.S., Bidirectional modulation of scopolamine-induced working memory impairments by muscarinic activation of the medial septal area, Neurobiol. Learning Memory, 63 (1995) 269-276.
73. Givens, B., Olton, D.S. and Crawley, J., Galanin in the medial septal area impairs working memory. Brain Res., 582 (1992) 71-77.
74. Givens, B.S. and Breese, G.R., Site-specific enhancement of gamma-aminobutyric acid-mediated inhibition of neural activity by ethanol in the rat medial septal area, J. Pharmacol. Exp. Ther., 254 (1990) 528-538.
75. Gorman, L.K., Pang, K., Frick, K.M., Givens, B. and Olton, D.S., Acetylcholine release in the hippocampus: Effects of cholinergic and GABAergic compounds in the medial septal area, Neurosci. Lett., 166 (1994) 199-202.
76. Gray, J.A., The Neuropsychology of Anxiety: An Enquiry into the Functions of the Septo-hippocampal System, Oxford University Press, Oxford, 1982,
77. Gray, J.A. and McNaughton, N., Comparison between the behavioral effects of septal and hippocampal lesions: A review, Neurosci. Biobehav. Rev., 7 (1983) 119-188.
78. Green, J.D. and Arduini, A., Hippocampal electrical activity in arousal, J. Neurophysiol, 17 (1954) 533-557.
79. Grove, E.A., Efferent connections of the substantia innominata in the rat, J. Comp. Neural., 277 (1988) 347-364.
80. Hasselmo, M.E., Neuromodulation and cortical function: modeling the physiological basis of behavior, Behav. Brain Res., 67 (1995) 1-27.
81. Heckers, S. and Mesulam, M.-M., Two types of cholinergic projections to the rat amygdala, Neuroscience, 60 (1994) 383-397.
82. Hepler, D., Olton, D.S., Wenk, G.L. and Coyle, J.T., Lesions in nucleus basalis magnocellularis and medial septal area of rats produce qualitatively similar memory impairments, J. Neurosci., 5 (1985) 866-873.
83. Himmelheber, A.-M., Moore, H., McGaughy, J., Givens, B., Bruno, J.P. and Sarter, M., Cortical acetylcholine efflux and single unit activity in rats performing operant procedures assessing behavioral vigilance, or sensorimotor and motivational task components, Soc. Neurosci. Abstr., 21 (1995) 763.6
84. Holley, L.A., Turchi, J., Apple, C. and Sarter, M., Dissociation between the attentional effects of infusions of a benzodiazepine receptor agonist and an inverse agonist into the basal forebrain, Psychopharmacology, 120 (1995) 99-108.
85. Hooks, M.S. and Kalivas, P.W., Involvement of dopamine and excitatory amino acid transmission in novelty-induced motor activity, J. Pharmacol. Exp. Ther., 269 (1994) 976-988.
86. Ingham, C.A., Bolam, J.P. and Smith, A.D., GABA-immunoreactive synaptic boutons in the rat basal forebrain: Comparison of neurons that project to the neocortex with pallidosubthalamic neurons. J. Comp. Neural, 273 (1988) 263-282.
87. Inglis, P.M., Day, J.C. and Fibiger, H.C., Enhanced acetylcholine release in hippocampus and cortex during the anticipation and consumption of a palatable meal. Neuroscience, 62 (1994) 1049-1056.
88. Jaffard, R., Marighetto, A. and Micheau, J., Septal noradrenergic and glutamatergic influences on hippocampal cholinergic activity in relation to spatial learning and memory in mice. In E.D. Levin, M.W. Decker and L.L. Butcher (Eds.) Neurotransmitter interactions and cognitive function, Birkhauser, Boston, 1992, pp. 103-117.
89. Jakab, R.L. and Leranth, C, Catecholaminergic, GABAergic, and hippocamposeptal innervation of GABAergic 'somatospiny' neurons in the rat lateral septal area, J. Comp. Neural., 302 (1990) 305-321.
90. Joels, M. and Urban, I.J.A., Electrophysiological and pharmacological evidence in favor of amino acid neurotransmission in fimbria-fornix fibers innervating the lateral septal complex of the rat, Exp. Brain Res., 54 (1984) 455-462.
91. Joels, M. and Urban, I.J.A., Monoamine-induced responses in lateral septal neurons: influence of iontophoretically applied vasopressin, Brain Res., 344 (1985) 120-126.
92. Jones, B.E. and Cuello, A.C., Afferents to the basal forebrain cholinergic cell area from pontomesencephalic-catecholamine, serotonin, and acetylcholine-neurons, Neuroscience, 31 (1989) 37-61.
93. Kalivas, P.W, Klitenick, M.A., Hagler, H. and Austin, M.C., GABAergic and enkephalinergic regulation of locomotion in the ventral pallidum: Involvement of the mesolimbic dopamine system, Adv. Exp. Med. Biol., 295 (1991) 315-326.
94. Kesner, R.P., Crutcher, K. and Omana, H., Memory deficits following nucleus basalis magnocellularis lesions may be mediated through limbic, but not neocortical, targets, Neuroscience, 38 (1990) 93-102.
95. Kesner, R.P., Crutcher, K.A. and Measom, M.O., Medial septal and nucleus basalis magnocellularis lesions produce order memory deficits in rats which mimic symptomatology of Alzheimer's disease, Neurobiol. Aging, 7 (1986) 287-295.
96. Koch, M., The septohippocampal system is involved in prepulse inhibition of the acoustic startle response in rats, Behav. Neurosci., 110 (1996) 468-477.
97. Kodsi, M.H. and Swerdlow, N.R., Ventral pallidal GABA-A receptors regulate prepulse inhibition of acoustic startle, Brain Res., 684 (1995) 26-35.
98. Koliatsos, V.E. and Price, D.L., The basal forebrain cholinergic system: An evolving concept in the neurobiology of the forebrain. In R.T. Richardson (Ed.) Activation to Acquisition: Functional Aspects of the Basal Forebrain Cholinergic System, Birkhauser, Boston, 1991, pp. 11-71.
99. Lamour, Y., Dutar, P. and Jobert, A., Septo-hippocampal and other medial septum-diagonal band neurons: Electrophysiological and pharmacological properties, Brain Res., 309 (1984) 227-239.
100. Lamour, Y., Dutar, P., Rascol, O. and Jobert, A., Basal forebrain neurons projecting to the rat frontoparietal cortex: electrophysiological and pharmacological properties, Brain Res., 362 (1986) 121-131.
101. Landgraf, R., Gerstberger, R., Montkowski, A., Probst, J.C., Wotjak, C.T., Holsboer, F. and Engelmann, M., V1 vasopressin receptor antisense oligodeoxynucleotide into the septum reduces vasopressin binding, social discrimination abilities, and anxiety-related behavior in rats, J. Neurosci., 15 (1995) 4250-4258.
102. Lawson, V.H. and Bland, B.H., The role of the septohippocampal pathway in the regulation of hippocampal field activity and behavior: Analysis by the intraseptal microinfusion of carbachol, atropine, and procaine, Exp. Neural., 120 (1993) 132-144.
103. Leranth, C., Deller, T. and Buzsáki, G., Intraseptal connections redefined: Lack of a lateral septum to medial septum path, Brain Res., 583 (1992) 1-11.
104. Leranth, C. and Frotscher, M., Organization of the septal region in the rat brain: Cholinergic-GABAergic interconnections and the termination of hippocampo-septal fibers, J. Comp. Neural., 289 (1989) 304-314.
105. Levey, A.I., Hallanger, A.E. and Wainer, B.H., Cholinergic nucleus basalis neurons may influence the cortex via the thalamus, Neurosci. Lett., 74 (1987) 7-13.
106. Marighetto, A., Micheau, J. and Jaffard, R., Effects of intraseptally injected glutamatergic drugs on hippocampal sodium-dependent high-affinity choline uptake in 'naive' and 'trained' mice, Pharmacol. Biochem. Behav., 49 (1994) 689-699.
107. Markowska, A.L., Olton, D.S. and Givens, B., Cholinergic manipulations in the medial septal area: age-related effects on working memory and hippocampal electrophysiology, J. Neurosci., 15 (1995) 2063-2073.
108. Martin, L.J., Blackstone, C.D., Levey, A.I., Huganir, R.L. and Price, D.L., Cellular localization of AMPA glutamate receptors within the basal forebrain magnocellular complex of rat and monkey, J. Neurosci., 13 (1993) 2249-2263.
109. Mayo, W., Dellu, F., Cherkaoui, J, Chapouthier, G., Dodd, R.H., LeMoal, M. and Simon, H., Cognitive enhancing properties of beta-CCM infused into the nucleus basalis magnocellularis of the rat, Brain Res., 589 (1992) 109-114.
110. McCormick, D.A. and Prince, D.A., Mechanisms of action of acetylcholine in the guinea-pig cerebral cortex in vitro, J. Physiol., 375 (1986) 169-194.
111. McDonald, R.J. and White, N.M., A triple dissociation of memory systems: Hippocampus, amygdala, and dorsal striatum, Behav. Neurosci., 107 (1993) 3-22.
112. McGaugh, J.L., Introini-Collison, I., Cahill, L.F., Castellano, C., Dalmaz, C., Parent, M.B. and Williams, C.L., Neuromodulatory systems and memory storage: role of the amygdala, Behav. Brain Res., 58 (1993) 81-90.
113. McGaughy, J., Kaiser, T. and Sarter, M., Behavioral vigilance following infusions of 192 IgG-saporin into the basal forebrain: selectivity of the behavioral impairment and relation to cortical AChE-positive fiber density, Behav. Neurosci. 110 (1996) 247-265.
114. McGaughy, J. and Sarter, M., Interactions between the attentional effects of intrabasalis infusions of BXR agonists and inverse agonists and systemic haloperidol, Soc. Neurosci. Abstr., 21 (1995) 763.5
115. McGaughy, J. and Sarter, M., Behavioral vigilance in rats: task validation and effects of age, amphetamine, and benzodiazepine receptor ligands, Psychopharmacology, 117 (1995) 340-357.
116. McLennan, H. and Miller, J.J., Gamma-aminobutyric acid and inhibition of the septal nuclei of the rat, J. Physiol., 237 (1974) 625-633.
117. McNamara, R.K. and Skelton, R.W., Effects of intracranial infusions of chlordiazepoxide on spatial learning in the Morris water maze. II. Neuropharmacological specificity, Behav. Brain Res., 59 (1993) 193-204.
118. McNamara, R.K. and Skelton, R.W., Effects of intracranial infusions of chlordiazepoxide on spatial learning in the Morris water maze. I. Neuroanatomical specificity, Behav. Brain Res., 59 (1993) 175-191.
119. Meek, W.H., Church, R.M., Wenk, G.L. and Olton, D.S., Nucleus basalis magnocellularis and medial septal area lesions differentially impair temporal memory, J. Neurosci., 7 (11) (1987) 3505-3511.
120. Melander, T., Hökfelt, T. and Rokaeus, A., Distribution of galanin-like immunoreactivity in the rat central nervous system, J. Comp. Neural, 248 (1986) 475-517.
121. Mesulam, M.-M., Hersh, L.B., Mash, D.C. and Geula, C., Differential cholinergic innervation within functional subdivisions of the human cerebral cortex: A choline acetyltransferase study, J. Comp. Neural., 318 (1992) 316-328.
122. Mesulam, M.-M., Mufson, E.J., Wainer, B.H. and Levey, A.I., Central cholinergic pathways in the rat: An overview based on an alternative nomenclature, Neuroscience, 10 (1983) 1185-1201.
123. Milner, T.A., Kurucz, O.S., Veznedaroglu, E. and Pierce, J.P. Septohippocampal neurons in the rat septal complex have substantial glial coverage and receive direct contacts from noradrenaline terminals, Brain Res., 670 (1995) 121-136.
124. Mizumori, S.J.Y., McNaughton, B.L., Barnes, C.A. and Fox, K.B., Preserved spatial coding in hippocampal CA1 pyramidal cells during reversible suppression of CA3c output: Evidence for pattern completion in hippocampus, J. Neurosci., 9 (1989) 3915-3928.
125. Mogenson, G.J., Swanson, L.W. and Wu, M., Neural projections from nucleus accumbens to globus pallidus, substantia innominata, and lateral preoptic-lateral hypothalamic area: an anatomical and electrophysiological investigation in the rat, J. Neurosci., 3 (1983) 189-202.
126. Mogenson, G.J. and Yang, C.R., The contribution of basal forebrain to limbic-motor integration and the mediation of motivation to action, Adv. Exp. Med. Biol, 295 (1991) 267-290.
127. Monmaur, P., Puma, C. and Sharif, A., Involvement of M2 and non-M2 muscarinic receptors in hippocampal theta rhythm induced by carbachol infusion into the septum of the rat, Brain Res., 656 (1994) 199-204.
128. Moor, E., De Boer, P., Beldhuis, H.J.A. and Westerink, B.H.C., A novel approach for studying septo-hippocampal cholinergic neurons in freely moving rats: A microdialysis study with dualprobe design, Brain Res., 648 (1994) 32-38.
129. Moore, H., Dudchenko, P., Comer, K.S., Bruno, J.P. and Sarter, M., Central versus peripheral effects of muscarnic antagonists: The limitations of quaternary ammonium derivitives, Psychopharmacology, 108 (1992) 241-243.
130. Moore, H., Sarter, M. and Bruno, J.P., Bidirectional modulation of cortical acetylcholine efflux by infusion of benzodiazepine receptor ligands into the basal forebrain, Neurosci. Lett., 189 (1995) 31-34.
131. Moore, H., Sarter, M. and Bruno, J.P., Interactions between benzodiazepine and dopamine receptors in the modulation of cortical acetylcholine release, Soc. Neurosci. Abstr., 21 (1995) 763.1
132. Moore, R.Y., Catecholamine innervation of the basal forebrain: the septal area, J. Comp. Neural., 177 (1978) 665-684.
133. Muir, J.L., Robbins, T.W. and Everitt, B.J., Disruptive effects of muscimol infused into the basal forebrain on conditional discrimination and visual attention: Differential interactions with cholinergic mechanisms, Psychopharmacology, 107 (1992) 541-550.
134. Nagahara, A.M., Brioni, J.D. and McGaugh, J.L., Effects of intraseptal infusion of muscimol on inhibitory avoidance and spatial learning: Differential effects of pretraining and posttraining administration, Psychobiology, 20 (1992) 198-204.
135. Nagahara, A.H. and McGaugh, J.L., Muscimol infused into the medial septal area impairs long-term memory but not short-term memory in inhibitory avoidance, water maze place learning and rewarded alternation tasks, Brain Res., 591 (1992) 54-61.
136. Nagel, J.A. and Huston, J.P., Enhanced inhibitory avoidance learning produced by post-trial injections of substance P into the basal forebrain, Behav. Neural Biol., 49 (1988) 374-385.
137. Napier, T.C., Functional pharmacology of basal forebrain dopamine. In E.D. Levin, M.W. Decker and L.L. Butcher (Eds.) Neurotransmitter Interactions and Cognitive Function, Birkhauser, Boston, 1992, pp. 66-77.
138. Napier, T.C. and Maslowski-Cobuzzi, R.J., Electrophysiological verification of the presence of D1 and D2 dopamine receptors within the ventral pallidum, Synapse, 17 (1994) 160-166.
139. Napier, T.C., Mitrovic, I., Churchill, L., Klitenick, M.A., Lu, X.Y. and Kalivas, P.W., Substance P in the ventral pallidum: Projection from the ventral striatum, and electrophysiological and behavioral consequences of pallidal substance P, Neuroscience, 69 (1995) 59-70.
140. Napier, T.C., Muench, M.B., Maslowski, R.J. and Battaglia, G., Is dopamine a neurotransmitter within the ventral pallidum/ substantia innominata, Adv. Exp. Med. Biol. 295 (1991) 183-195.
141. Nilsson, O.G., Kalen, P., Rosengren, E. and Björklund, A., Ace-tylcholine release in the rat hippocampus as studied by microdialysis is dependent on axonal impulse flow and increases during behavioral activation, Neuroscience, 36 (1990) 325-338.
142. Olton, D., Experimental strategies to identify the neurobiological basis of memory: Lesions. In J.L. Martinez and R.P. Kesner (Eds.), Learning and Memory: A Biological View, Academic Press, New York, 1991, pp. 441-466.
143. Olton, D.S., Givens, B., Markowska, A.L., Shapiro, M.L. and Golski, S., Mnemonic functions of the cholinergic septohippocampal system. In L.R. Squire, N.M. Weinberger, G. Lynch and J.L. McGaugh (Eds.) Memory: Organization and Locus of Change, Oxford University Press, New York, 1991, pp. 250-269.
144. Olton, D.S. and Wenk, G.L., Dementia: Animal models of the cognitive impairments produced by degeneration of the basal forebrain cholinergic system. In H.Y. Meltzer (Ed.) Psychopharmacology: The Third Generation of Progress, Raven Press, New York, 1987, pp. 941-953.
145. Osborne, P.G., A GABAergic mechanism in the medial septum influences cortical arousal and locomotor activity but not a previously learned spatial discrimination task, Neurosci. Lett., 173 (1994) 63-66.
146. Page, K.J., Sirinathsinghji, D.J.S. and Everitt, B.J., AMPA-induced lesions of the basal forebrain differentially affect cholinergic and non-cholinergic neurons: Lesion assessment using quantitative in situ hybridization histochemistry, Eur. J. Neurosci., 7 (1995) 1012-1021.
147. Palmer, A.M., Francis, P.T., Benton, J.S., Sims, N.R., Mann, D.M.A., Neary, D., Snowden, J.S. and Bowen, D.M., Presynaptic serotonergic dysfunction in patients with Alzheimer's disease, J. Neurochem., 48 (1987) 8-15.
148. Palmer, A.M., Francis, P.T., Bowen, D.M., Benton, J.S., Neary, D., Mann, D.M.A. and Snowden, J.S., Catecholaminergic neurones assessed ante-mortem in Alzheimer's disease, Brain Res., 414 (1987) 365-375.
149. Pang, K., Williams, M.J., Egeth, H. and Olton, D.S., Nucleus basalis magnocellularis and attention: Effects of muscimol infusions, Behav. Neurosci., 107 (1993) 1031-1038.
150. Pang, K., Williams, M.J. and Olton, D.S., Activation of the medial septal area attenuates LTP of the lateral perforant path and enhances heterosynaptic LTD of the medial perforant path in aged rats, Brain Res., 632 (1993) 150-160.
151. Pesold, C. and Treit, D., The septum and amygdala differentially mediate the anxiolytic effects of benzodiazepines, Brain Res., 638 (1994) 295-301.
152. Ragozzino, M.E., Parker, M.E. and Gold, P.E., Spontaneous alternation and inhibitory avoidance impairments with morphine injections into the medial septum. Attenuation by glucose administration, Brain Res., 597 (1992) 241-249.
153. Rajkowski, J., Kubiak, P. and Aston-Jones, G., Locus coeruleus activity in monkey: Phasic and tonic changes are associated with altered vigilance, Brain Res. Bull., 35 (1994) 607-616.
154. Rasmusson, D.D., Clow, K. and Szerb, J.C., Modification of neocortical acetylcholine release and electroencephalogram desynchronization due to brainstem stimulation by drugs applied to the basal forebrain, Neuroscience, 60 (1994) 665-677.
155. Rex, A., Marsden, C.A. and Fink, H., Effect of diazepam on cortical 5-HT release and behavior in the guinea-pig on exposure to the elevated plus maze, Psychopharmacology, 110 (1993) 490-496.
156. Richardson, R.T. and DeLong, M.R., Context-dependent responses of primate nucleus basalis neurons in a go/no-go task, J. Neurosci., 10 (1990) 2528-2540.
157. Richardson, R.T. and DeLong, M.R., Electrophysiological studies of the functions of the nucleus basalis in primates. In T.C. Napier, P.W. Kalivas and I. Hanin (Eds.) The Basal Forebrain: Anatomy to Function, Plenum Press, New York, 1991, pp. 233-252.
158. Rieck, R.W., Nabors, C.C., Updyke, B.V. and Kratz, K.E., Organization of the basal forebrain in the cat: localization of L-enkephalin, substance P, and choline acetyltransferase immunoreactivity, Brain Res., 672 (1995) 237-250.
159. Riekkinen, P., Buzsáki, G., Riekkinen, P., Jr., Soininen, H. and Partanen, J., The cholinergic system and EEG slow waves, Electroenceph. Clin. Neurophysiol, 78 (1991) 89-96.
160. Robbins, T.W. and Everitt, B.J., Arousal systems and attention. In M.S. Gazzaniga (Ed.) The Cognitive Neurosciences, MIT Press, Cambridge, 1995, pp. 703-720.
161. Robbins, T.W., Everitt, B.J., Marston, H.M., Wilkinson, J., Jones, G.H. and Page, K.J., Comparative effects of ibotenic acid and quisqualic acid-induced lesions of the substantia innominata on attentional function in the rat: Further implications for the role of the cholinergic neurons of the nucleus basalis in cognitive processes. Behav. Brain Res., 35 (1989) 221-240.
162. Robinson, J.K. and Crawley, J.N., Intraseptal galanin potentiates scopolamine impairment of delayed non-match to sample, J. Neurosci., 13 (1993) 5119-5125.
163. Robinson, J.K. and Crawley, J.N., Analysis of anatomical sites at which galanin impairs delayed nonmatching to sample in rats, Behav. Neurosci., 108 (1994) 941-950.
164. Robinson, S.E., Hambrecht, K.L. and Lyeth, B.G., Basal forebrain carbachol injection reduces cortical acetylcholine turnover and disrupts memory, Brain Res., 445 (1988) 160-164.
165. Robinson, S.E., Mathe-Sorenssen, D., Wood, P.L. and Commissiong, J., Dopaminergic control of the septal-hippocampal cholinergic pathway, J. Pharmacol. Exp. Ther., 208 (1979) 476-479.
166. Routtenberg, A., Intracranial chemical injection and behavior: A critical review, Behav. Biol., 7 (1972) 601-641.
167. Russchen, F.T., Amaral, D.G. and Price, J.L., The afferent connections of the substantia innominata in the monkey, Macaca fascicularis, J. Comp. Neural., 242 (1985) 1-27.
168. Sarter, M., Neuronal mechanisms of the attentional dysfunctions in senile dementia and schizophrenia: two sides of the same coin? Psychopharmacology, 114 (1994) 539-550.
169. Sarter, M. and Bruno, J.P., Cognitive functions of cortical ACh: lessons
170. Sarter, M. and Bruno, J.P., Trans-synaptic stimulation of cortical acetylcholine and attention: A rational approach for the development of cognition enhancers, Behav. Brain Res. (1996), in press.
171. Sarter, M. and Bruno, J.P., Cortical acetylcholine, attention, and neuropharmacological and cognitive principles or a rational development of treatment strategies for cognitive disorders. In J.E. Brioni and M.W. Decker (Eds.), Alzheimer's Disease: Molecular Aspects and Pharmacological Treatments, John Wiley, New York, 1996, in press.
172. Sarter, M. and Bruno, J.P., Cognitive functions of cortical acetylcholine: towards a unifying hypothesis, Brain Res. Rev., (1996), in press.
173. Sarter, M., Bruno, J.P. and Dudchenko, P., Activating the damaged basal forebrain cholinergic system: tonic stimulation versus signal amplification, Psychopharmacology, 101 (1990) 1-17.
174. Sarter, M., Bruno, J.P., Givens, B., Moore, H., McGaughy, J. and McMahon, K., Neuronal mechanisms of drug effects on cognition: cognitive activity as a necessary intervening variable, Cog. Brain Res., 3 (1996) 329-343.
175. Sarter, M., Hagan, J. and Dudchenko, P., Behavioral screening for cognitive enhancers: from indiscriminate to valid testing: Part I, Psychopharmacology, 107 (1992) 144-159.
176. Sarter, M., Hagan, J. and Dudchenko, P., Behavioral screening for cognitive enhancers: from indiscriminate to valid testing: Part II, Psychopharmacology, 107 (1992) 461-473.
177. Sarter, M. and Markowitsch, H.J., Involvement of the amygdala in learning and memory: A critical review with emphasis on anatomical relations, Behav. Neurosci., 99 (1985) 342-380.
178. Sarter, M., Nutt, D.J. and Lister, R., Benzodiazepine Receptor Inverse Agonists, John Wiley & Sons, New York, 1994.
179. Semba, K., The cholinergic basal forebrain: A critical role in cortical arousal, Adv. Exp. Med. Biol, 295 (1991) 197-218.
180. Simon, H., Taghzouti, K. and LeMoal, M., Deficits in spatial-memory tasks following lesions of septal dopaminergic terminals in the rat, Behav. Brain Res., 19 (1986) 7-16.
181. Smith, C.G., Beninger, R.J., Mallet, P.E., Jhamandas, K. and Boegman, R.J., Basal forebrain injections of the benzodiazepine partial inverse agonist FG 7142 enhance memory of rats in the double Y-maze, Brain Res., 666 (1994) 61-67.
182. Stackman, R.W. and Walsh, T.J., Chlordiazepoxide-induced working memory impairments: Site specificity and reversal by flumazenil (RO15-1788), Behav. Neural Biol., 57 (1992) 233-243.
183. Stackman, R.W. and Walsh, T.J., Baclofen produces dose-related working memory impairments after intraseptal injection, Behav. Neural Biol., 61 (1994) 181-185.
184. Staubli, U. and Huston, J.P., Central actions of substance P: possible role in reward, Behav. Neural Biol., 43 (1985) 100-108.
185. Swanson, L.W., Kohler, C. and Björklund, A., The limbic region. I. The septohippocampal system. In A. Björklund and T. Hökfelt (Eds.), Handbook of chemical neuroanatomy, Elsevier, Amsterdam, 1987, pp. 125-276.
186. Swanson, L.W., Sawchenko, P.E. and Cowan, W.M., Evidence that the commissural, associational, and septal projections of the regio inferior of the hippocampus arise from the same neurons, Brain Res., 197 (1980) 207-212.
187. Sweeney, I.E., Lamour, Y. and Bassant, M.H., Arousal-dependent properties of medial septal neurons in the unanesthetized rat, Neuroscience, 48 (1992) 353-362.
188. Szeidemann, Z., Shanabrough, M. and Leranth, C., Hypothalamic Leu-enkephalin-immunoreactive fibers terminate on calbindin-containing somatospiny cells in the lateral septal area of the rat, J. Comp. Neural., 358 (1995) 573-583.
189. Szerb, J.C., Clow, K. and Rasmusson, D.D., Pharmacological but not physiological modulation of cortical acetylcholine release by cholinergic mechanisms in the nucleus basalis magnocellularis, Can. J. Physiol. Pharmacol., 12 (1994) 893-898.
190. Szigethy, E. and Beaudet, A., Selective association of neurontensin receptor with cholinergic neurons in the rat basal forebrain, Neurosci. Lett., 83 (1987) 47-52.
191. Taylor, J.L. and Tinklenberg, J.R., Cognitive impairment and benzodiazepines. In H.Y. Meltzer (Ed.), Psychopharmacology: The Third Generation of Progress, Raven Press, New York, 1987, pp. 1449-1454.
192. Tóth, K., Borhegyi, Z. and Freund, T.F., Postsynaptic targets of GABAergic hippocampal neurons in the medial septum-diagonal band of Broca complex, J. Neurosci., 13 (1993) 3712-3724.
193. Trembley, N., Warren, R.A. and Dykes, R.W., Electrophysiological studies of acetylcholine and the role of the basal forebrain in the somatosensory cortex of the cat II. Cortical neurons excited by somatic stimuli, J. Neurophysiol., 64 (1990) 1212-1222.
194. Turchi, J., Bruno, J.P. and Sarter, M., Cortical acetylcholine and processing capacity: effect of cortical cholinergic deafferentation on crossmodal divided attention in rats, Soc. Neurosci. Abstr., 21 (1995) 763.9 (Abstract).
195. Urban, U.A., Intraseptal administration of vasopressin and oxytocin affects hippocampal electroencephalogram in rats, Exp. Neural., 74 (1981) 131-147.
196. Van der Zee, E.A. and Luiten, P.G.M., Cholinergic and GABAergic neurons in the rat medial septum express muscarinic acetylcholine receptors, Brain Res., 652 (1994) 263-272.
197. Vertes, R.P., Brainstem afferents to the basal forebrain in the rat, Neuroscience, 24 (1988) 907-935.
198. Voytko, M.L., Olton, D.S., Richardson, R.T., Gorman, L.K., Tobin, J.R. and Price, D.L., Basal forebrain lesions in monkeys disrupt attention but not learning and memory, J. Neurosci., 14 (1994) 167-186.
199. Waite, J.J., Chen, A.D., Wardlow, M.L., Wiley, R.G., Lappi, D.A. and Thal, L.J., 192 immunoglobulin G-saporin produces graded behavioral and biochemical changes accompanying the loss of cholinergic neurons of the basal forebrain and cerebellar Purkinje cells, Neuroscience, 65 (1995) 463-476.
200. Wallace, L.J. and Uretsky, N.J., Effect of GABAergic and glutamatergic drugs injected into the ventral pallidum on locomotor activity, Adv. Exp. Med. Biol., 295 (1991) 307-314.
201. Walsh, T.J. and Stackman, R.W., Modulation of memory by benzodiazepine-acetylcholine interactions. In E.D. Levin, M.W. Decker and L.L. Butcher (Eds.), Neurotransmitter Interactions and Cognitive Function, Birkhauser, Boston, 1992, pp. 312-328.
202. Walsh, T.J., Stackman, R.W., Emerich, D.F. and Taylor, L.A., Intraseptal injection of GABA and benzodiazepine receptor ligands alters high-affinity choline transport in the hippocampus, Brain Res. Bull., 31 (1993) 267-271.
203. Wan, R.-Q., Givens, B. and Olton, D.S., Opiod modulation of working memory: Intraseptal, but not intraamygdala, infusions of B-endorphin impair performance in spatial alternation, Neurobiol. Learning Memory, 63 (1995) 74-86.
204. Wenk, G.L., The influence of neurotensin upon cholinergic function. In E.D. Levin, M.W. Decker and L.L. Butcher (Eds.) Neurotransmitter Interactions and Cognitive Function, Birkhauser, Boston, 1992, pp. 196-206.
205. 3H] choline into acetylcholinergic neurons of the nucleus basalis magnocellularis and medial septal area, Behav. Brain Res., 13 (1984) 129-138.
206. Wenk, G.L., Stoehr, J.D., Quintana, G., Mobley, S. and Wiley, R.G., Behavioral, biochemical, histological, and electrophysiological effects of 192 IgG-saporin injections into the basal forebrain of rats, J. Neurosci., 14 (1994) 5986-5995.
207. Whalen, P.J., Neuronal activity with the nucleus basalis and conditioned neocortical electroencephalographic activation, J. Neurosci., 14 (1994) 1623-1633.
208. Whitehouse, P.J., Price, D.L., Struble, R.G., Clark, A.W., Coyle, J.T. and DeLong, M.R., Alzheimer's disease and senile dementia: Loss of neurons in the basal forebrain, Science, 215 (1982) 1237-1239.
209. Wilson, F.A.W. and Rolls, E.T., Neuronal responses related to the novelty and familiarity of visual stimuli in the substantia innominata, diagonal band of Broca and periventricular region of the primate basal forebrain, Exp. Brain Res., 80 (1990) 104-120.
210. Witter, M.P., Daelmans, H.E.M., Jorritsma-Byham, B., Staiger, J.F. and Wouterlood, F.G., Restricted origin and distribution of projections from the lateral to the medial septal complex in rat and guinea pig, Neurosci. Lett., 148 (1992) 164-168.
211. Woolf, N.J. and Butcher, L.L., Cholinergic systems in the rat brain, III. Projections from the pontomesencephalic tegmentum to the thalamus, tectum, basal ganglia, and basal forebrain, Brain Res. Bull., 16 (1986) 603-637.
212. Wright, I.K., Upton, N. and Marsden, C.A., Effect of established and putative anxiolytics on extracellular 5-HT and 5-HIAA in the ventral hippocampus of rats during behavior on the elevated X-maze, Psychopharmacology, 109 (1992) 338-346.
213. Zaborszky, L. and Cullinan, W.E., Projections from the nucleus accumbens to cholinergic neurons of the ventral pallidum: a correlated light and electron microscopic double-immunolabeling study in rat, Brain Res., 570 (1992) 92-101.
214. Zaborszky, L. and Cullinan, W.E., Direct catecholaminergic-cholinergic interactions in the basal forebrain. I. Dopamine-beta-hydroxylase and tyrosine-hydroxylase input to cholinergic projection neurons, J. Comp. Neural. (1996), in press.
215. Zaborszky, L, Cullinan, W.E. and Braun, A., Afferents to basal forebrain cholinergic projection neurons: an update, Adv. Exp. Med. Biol., 295 (1991) 43-100.
216. Zaborszky, L., Heimer, L., Eckenstein, F. and Leranth, C., GABAergic input to cholinergic forebrain neurons: an ultra-structural study using retrograde tracing of HRP and double immunolabeling, J. Comp. Neural., 250 (1986) 282-295.
217. Zilles, K., Werner, L., Qu, M., Schleicher, A. and Gross, G., Quantative autoradiography of 11 different transmitter binding sites in the basal forebrain region of the rat - evidence of heterogeneity in distribution patterns, Neuroscience, 42 (1991) 473-481.