Regulation of cortical acetylcholine release: Insights from in vivo microdialysis studies

Behavioural Brain Research

Volumn 221, Issue 2, 2011, Pages 527-536

  Fadel, Jim R ^a  

^a UNIVERSITY OF SOUTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Acetylcholine; Basal forebrain; Cerebral cortex; Microdialysis; Neurotransmitter release

Indexed keywords

AMYLOID BETA PROTEIN; ARGIPRESSIN; DYNORPHIN A; NEUROTENSIN; PROTIRELIN; SUBSTANCE P;

ACETYLCHOLINE RELEASE; AGING; ALZHEIMER DISEASE; BRAIN CORTEX; CHOLINERGIC TRANSMISSION; COGNITION; CORTICAL SYNCHRONIZATION; ELECTROENCEPHALOGRAPHY PHASE SYNCHRONIZATION; FOREBRAIN; IN VIVO STUDY; MICRODIALYSIS; NEUROTRANSMISSION; NONHUMAN; PRESYNAPTIC MEMBRANE; PRIORITY JOURNAL; REVIEW; SCHIZOPHRENIA; SIGNAL TRANSDUCTION; TEGMENTUM; TRANSGENE; WORKING MEMORY;

ACETYLCHOLINE; AGING; ANIMALS; CENTRAL NERVOUS SYSTEM STIMULANTS; CEREBRAL CORTEX; CHOLINERGIC FIBERS; COGNITION; HUMANS; MENTAL DISORDERS; MICRODIALYSIS; MODELS, NEUROLOGICAL; NEURAL PATHWAYS; PRESYNAPTIC TERMINALS; PROSENCEPHALON; SYNAPTIC TRANSMISSION;

EID: 79955724638     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2010.02.022     Document Type: Review

References (168)

1. Acquas E., Marrocu P., Pisanu A., Cadoni C., Zernig G., Saria A., et al. Intravenous administration of ecstasy (3,4-methylendioxymethamphetamine) enhances cortical and striatal acetylcholine release in vivo. Eur J Pharmacol 2001, 418:207-211.
2. Acquas E., Tanda G., Di Chiara G. Differential effects of caffeine on dopamine and acetylcholine transmission in brain areas of drug-naive and caffeine-pretreated rats. Neuropsychopharmacology 2002, 27:182-193.
3. Alexander K.S., Brooks J.M., Sarter M., Bruno J.P. Disruption of mesolimbic regulation of prefrontal cholinergic transmission in an animal model of schizophrenia and normalization by chronic clozapine treatment. Neuropsychopharmacology 2009, 34:2710-2720.
4. 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 2002, 114:451.
5. Arnold H.M., Fadel J., Sarter M., Bruno J.P. Amphetamine-stimulated cortical acetylcholine release: role of the basal forebrain. Brain Res 2001, 894:74-87.
6. Arnold H.M., Nelson C.L., Neigh G.N., Sarter M., Bruno J.P. Systemic and intra-accumbens administration of amphetamine differentially affects cortical acetylcholine release. Neuroscience 2000, 96:675-685.
7. Arnold H.M., Nelson C.L., Sarter M., Bruno J.P. Sensitization of cortical acetylcholine release by repeated administration of nicotine in rats. Psychopharmacology (Berl) 2003, 165:346-358.
8. Auchus A.P., Green R.C., Nemeroff C.B. Cortical and subcortical neuropeptides in Alzheimer's disease. Neurobiol Aging 1994, 15:589-595.
9. Barbelivien A., Vaussy C., Marchalant Y., Maubert E., Bertrand N., Beley A., et al. Degeneration of the basalocortical pathway from the cortex induces a functional increase in galaninergic markers in the nucleus basalis magnocellularis of the rat. J Cereb Blood Flow Metab 2004, 24:1255-1266.
10. Basheer R., Strecker R.E., Thakkar M.M., McCarley R.W. Adenosine and sleep-wake regulation. Prog Neurobiol 2004, 73:379-396.
11. Bertorelli R., Forloni G., Consolo S. Modulation of cortical in vivo acetylcholine release by the basal nuclear complex: role of the pontomesencephalic tegmental area. Brain Res 1991, 563:353-356.
12. Bigl V., Woolf N.J., Butcher L.L. Cholinergic projections from the basal forebrain to frontal, parietal, temporal, occipital, and cingulate cortices: a combined fluorescent tracer and acetylcholinesterase analysis. Brain Res Bull 1982, 8:727-749.
13. Blaker W.D. GABAergic control of the cholinergic projections to the frontal cortex is not tonic. Brain Res 1985, 325:389-390.
14. Boschen KE, Fadel JR, Burk JA. Systemic and intrabasalis administration of the orexin-1 receptor antagonist, SB-334867, disrupts attentional performance in rats, Psychopharmacology (Berl) 2009; 206:205-213.
15. Bourdelais A., Kalivas P.W. Amphetamine lowers extracellular GABA concentration in the ventral pallidum. Brain Res 1990, 516:132-136.
16. Brandon E.P., Mellott T., Pizzo D.P., Coufal N., D'Amour K.A., Gobeske K., et al. Choline transporter 1 maintains cholinergic function in choline acetyltransferase haploinsufficiency. J Neurosci 2004, 24:5459-5466.
17. Bruno J.P., Gash C., Martin B., Zmarowski A., Pomerleau F., Burmeister J., et al. Second-by-second measurement of acetylcholine release in prefrontal cortex. Eur J Neurosci 2006, 24:2749-2757.
18. Burmeister J.J., Pomerleau F., Huettl P., Gash C.R., Werner C.E., Bruno J.P., et al. Ceramic-based multisite microelectrode arrays for simultaneous measures of choline and acetylcholine in CNS. Biosens Bioelectron 2008, 23:1382-1389.
19. Butt A.E., Chavez C.M., Flesher M.M., Kinney-Hurd B.L., Araujo G.C., Miasnikov A.A., et al. Association learning-dependent increases in acetylcholine release in the rat auditory cortex during auditory classical conditioning. Neurobiol Learn Mem 2009, 92:400-409.
20. Carnes K.M., Fuller T.A., Price J.L. Sources of presumptive glutamatergic/aspartatergic afferents to the magnocellular basal forebrain in the rat. J Comp Neurol 1990, 302:824-852.
21. Casamenti F., Scali C., Pepeu G. Phosphatidylserine reverses the age-dependent decrease in cortical acetylcholine release: a microdialysis study. Eur J Pharmacol 1991, 194:11-16.
22. 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 Neurol 1988, 273:543-557.
23. Chan-Palay V. Alterations in the locus coeruleus in dementias of Alzheimer's and Parkinson's disease. Prog Brain Res 1991, 88:625-630.
24. Chew M.L., Mulsant B.H., Pollock B.G., Lehman M.E., Greenspan A., Kirshner M.A., et al. A model of anticholinergic activity of atypical antipsychotic medications. Schizophr Res 2006, 88:63-72.
25. Conn P.J., Jones C.K., Lindsley C.W. Subtype-selective allosteric modulators of muscarinic receptors for the treatment of CNS disorders. Trends Pharmacol Sci 2009, 30:148-155.
26. Consolo S., Bertorelli R., Forloni G.L., Butcher L.L. Cholinergic neurons of the pontomesencephalic tegmentum release acetylcholine in the basal nuclear complex of freely moving rats. Neuroscience 1990, 37:717-723.
27. Cornwell-Jones C.A., Decker M.W., Chang J.W., Cole B., Goltz K.M., Tran T., et al. Neonatal 6-hydroxydopa, but not DSP-4, elevates brainstem monoamines and impairs inhibitory avoidance learning in developing rats. Brain Res 1989, 493:258-268.
28. Crawley J.N. Minireview. Galanin-acetylcholine interactions: relevance to memory and Alzheimer's disease. Life Sci 1996, 58:2185-2199.
29. Cullinan W.E., Zaborszky L. Organization of ascending hypothalamic projections to the rostral forebrain with special reference to the innervation of cholinergic projection neurons. J Comp Neurol 1991, 306:631-667.
30. Dalley J.W., McGaughy J., O'Connell M.T., Cardinal R.N., Levita L., Robbins T.W. Distinct changes in cortical acetylcholine and noradrenaline efflux during contingent and noncontingent performance of a visual attentional task. J Neurosci 2001, 21:4908-4914.
31. Day J., Damsma G., Fibiger H.C. Cholinergic activity in the rat hippocampus, cortex and striatum correlates with locomotor activity: an in vivo microdialysis study. Pharmacol Biochem Behav 1991, 38:723-729.
32. Day J., Fibiger H.C. Dopaminergic regulation of cortical acetylcholine release. Synapse 1992, 12:281-286.
33. Day J.C., Piazza P.V., Le Moal M., Maccari S. Cocaine-induced increase in cortical acetylcholine release: interaction with the hypothalamo-pituitary-adrenal axis. Eur J Neurosci 1997, 9:1130-1136.
34. Day J.C., Tham C.S., Fibiger H.C. Dopamine depletion attenuates amphetamine-induced increases of cortical acetylcholine release. Eur J Pharmacol 1994, 263:285-292.
35. de Lecea L., Kilduff T.S., Peyron C., Gao X., Foye P.E., Danielson P.E., et al. The hypocretins: hypothalamus-specific peptides with neuroexcitatory activity. Proc Natl Acad Sci USA 1998, 95:322-327.
36. De Souza Silva M.A., Hasenohrl R.U., Tomaz C., Schwarting R.K., Huston J.P. Differential modulation of frontal cortex acetylcholine by injection of substance P into the nucleus basalis magnocellularis region in the freely-moving vs. the anesthetized preparation. Synapse 2000, 38:243-253.
37. Deller T., Sarter M. Effects of repeated administration of amphetamine on behavioral vigilance: evidence for " sensitized" attentional impairments. Psychopharmacology (Berl) 1998, 137:410-414.
38. Eckenstein F.P., Baughman R.W., Quinn J. An anatomical study of cholinergic innervation in rat cerebral cortex. Neuroscience 1988, 25:457-474.
39. Eggermann E., Serafin M., Bayer L., Machard D., Saint-Mleux B., Jones B.E., et al. Orexins/hypocretins excite basal forebrain cholinergic neurones. Neuroscience 2001, 108:177-181.
40. Elliott K.A., Swank R.L., Henderson N. Effects of anesthetics and convulsants on acetylcholine content of brain. Am J Physiol 1950, 162:469-474.
41. Espana R.A., Baldo B.A., Kelley A.E., Berridge C.W. Wake-promoting and sleep-suppressing actions of hypocretin (orexin): basal forebrain sites of action. Neuroscience 2001, 106:699-715.
42. Fadel J., Burk J.A. Orexin/hypocretin modulation of the basal forebrain cholinergic system: role in attention. Brain Res 2010, 1314:112-123.
43. Fadel J., Frederick-Duus D. Orexin/hypocretin modulation of the basal forebrain cholinergic system: insights from in vivo microdialysis studies. Pharmacol Biochem Behav 2008, 90:156-162.
44. Fadel J., Moore H., Sarter M., Bruno J.P. Trans-synaptic stimulation of cortical acetylcholine release after partial 192 IgG-saporin-induced loss of cortical cholinergic afferents. J Neurosci 1996, 16:6592-6600.
45. Fadel J., Pasumarthi R., Reznikov L.R. Stimulation of cortical acetylcholine release by orexin A. Neuroscience 2005, 130:541-547.
46. Fadel J., Sarter M., Bruno J.P. Age-related attenuation of stimulated cortical acetylcholine release in basal forebrain-lesioned rats. Neuroscience 1999, 90:793-802.
47. Fadel J., Sarter M., Bruno J.P. Basal forebrain glutamatergic modulation of cortical acetylcholine release. Synapse 2001, 39:201-212.
48. Fischer W., Nilsson O.G., Bjorklund A. In vivo acetylcholine release as measured by microdialysis is unaltered in the hippocampus of cognitively impaired aged rats with degenerative changes in the basal forebrain. Brain Res 1991, 556:44-52.
49. Fort P., Khateb A., Pegna A., Muhlethaler M., Jones B.E. Noradrenergic modulation of cholinergic nucleus basalis neurons demonstrated by in vitro pharmacological and immunohistochemical evidence in the guinea-pig brain. Eur J Neurosci 1995, 7:1502-1511.
50. Fournier G.N., Semba K., Rasmusson D.D. Modality- and region-specific acetylcholine release in the rat neocortex. Neuroscience 2004, 126:257-262.
51. Frederick-Duus D., Guyton M.F., Fadel J. Food-elicited increases in cortical acetylcholine release require orexin transmission. Neuroscience 2007, 149:499-507.
52. Fritschy J.M., Grzanna R. Immunohistochemical analysis of the neurotoxic effects of DSP-4 identifies two populations of noradrenergic axon terminals. Neuroscience 1989, 30:181-197.
53. Gastard M., Jensen S.L., Martin J.R., Williams E.A., Zahm D.S. The caudal sublenticular region/anterior amygdaloid area is the only part of the rat forebrain and mesopontine tegmentum occupied by magnocellular cholinergic neurons that receives outputs from the central division of extended amygdala. Brain Res 2002, 957:207-222.
54. Gaykema R.P., van Weeghel R., Hersh L.B., Luiten P.G. Prefrontal cortical projections to the cholinergic neurons in the basal forebrain. J Comp Neurol 1991, 303:563-583.
55. Giovannelli L., Casamenti F., Scali C., Bartolini L., Pepeu G. Differential effects of amyloid peptides beta-(1-40) and beta-(25-35) injections into the rat nucleus basalis. Neuroscience 1995, 66:781-792.
56. Giovannini M.G., Bartolini L., Kopf S.R., Pepeu G. Acetylcholine release from the frontal cortex during exploratory activity. Brain Res 1998, 784:218-227.
57. Giovannini M.G., Casamenti F., Nistri A., Paoli F., Pepeu G. Effect of thyrotropin releasing hormone (TRH) on acetylcholine release from different brain areas investigated by microdialysis. Br J Pharmacol 1991, 102:363-368.
58. Grove E.A. Neural associations of the substantia innominata in the rat: afferent connections. J Comp Neurol 1988, 277:315-346.
59. Haring J.H., Wang R.Y. The identification of some sources of afferent input to the rat nucleus basalis magnocellularis by retrograde transport of horseradish peroxidase. Brain Res 1986, 366:152-158.
60. Hedou G., Homberg J., Martin S., Wirth K., Feldon J., Heidbreder C.A. Effect of amphetamine on extracellular acetylcholine and monoamine levels in subterritories of the rat medial prefrontal cortex. Eur J Pharmacol 2000, 390:127-136.
61. Herzog C.D., Nowak K.A., Sarter M., Bruno J.P. Microdialysis without acetylcholinesterase inhibition reveals an age-related attenuation in stimulated cortical acetylcholine release. Neurobiol Aging 2003, 24:861-863.
62. Himmelheber A.M., Fadel J., Sarter M., Bruno J.P. Effects of local cholinesterase inhibition on acetylcholine release assessed simultaneously in prefrontal and frontoparietal cortex. Neuroscience 1998, 86:949-957.
63. Himmelheber A.M., Sarter M., Bruno J.P. Increases in cortical acetylcholine release during sustained attention performance in rats. Brain Res Cogn Brain Res 2000, 9:313-325.
64. Hiramatsu M., Mori H., Murasawa H., Kameyama T. Improvement by dynorphin A (1-13) of galanin-induced impairment of memory accompanied by blockade of reductions in acetylcholine release in rats. Br J Pharmacol 1996, 118:255-260.
65. Holley L.A., Turchi J., Apple C., Sarter M. Dissociation between the attentional effects of infusions of a benzodiazepine receptor agonist and an inverse agonist into the basal forebrain. Psychopharmacology (Berl) 1995, 120:99-108.
66. Hyde T.M., Crook J.M. Cholinergic systems and schizophrenia: primary pathology or epiphenomena?. J Chem Neuroanat 2001, 22:53-63.
67. Ichikawa J., Dai J., O'Laughlin I.A., Fowler W.L., Meltzer H.Y. Atypical, but not typical, antipsychotic drugs increase cortical acetylcholine release without an effect in the nucleus accumbens or striatum. Neuropsychopharmacology 2002, 26:325-339.
68. Jimenez-Capdeville M.E., Dykes R.W. Daily changes in the release of acetylcholine from rat primary somatosensory cortex. Brain Res 1993, 625:152-158.
69. Jimenez-Capdeville M.E., Dykes R.W. Changes in cortical acetylcholine release in the rat during day and night: differences between motor and sensory areas. Neuroscience 1996, 71:567-579.
70. Jimenez-Capdeville M.E., Dykes R.W., Myasnikov A.A. Differential control of cortical activity by the basal forebrain in rats: a role for both cholinergic and inhibitory influences. J Comp Neurol 1997, 381:53-67.
71. Jones B.E., Cuello A.C. Afferents to the basal forebrain cholinergic cell area from pontomesencephalic - catecholamine, serotonin, and acetylcholine - neurons. Neuroscience 1989, 31:37-61.
72. Karube I., Yokoyama K., Tamiya E. Microbiosensors for acetylcholine and glucose. Biosens Bioelectron 1993, 8:219-228.
73. Khateb A., Fort P., Williams S., Serafin M., Jones B.E., Muhlethaler M. Modulation of cholinergic nucleus basalis neurons by acetylcholine and N-methyl-d-aspartate. Neuroscience 1997, 81:47-55.
74. Khateb A., Fort P., Williams S., Serafin M., Muhlethaler M., Jones B.E. GABAergic input to cholinergic nucleus basalis neurons. Neuroscience 1998, 86:937-947.
75. Kikuchi T., Wang Y., Shinbori H., Sato K., Okumura F. Effects of ketamine and pentobarbitone on acetylcholine release from the rat frontal cortex in vivo. Br J Anaesth 1997, 79:128-130.
76. Knox D., Sarter M., Berntson G.G. Visceral afferent bias on cortical processing: role of adrenergic afferents to the basal forebrain cholinergic system. Behav Neurosci 2004, 118:1455-1459.
77. Kuhar M.J., Murrin L.C. Sodium-dependent, high affinity choline uptake. J Neurochem 1978, 30:15-21.
78. Kurokawa M., Shiozaki S., Nonaka H., Kase H., Nakamura J., Kuwana Y. In vivo regulation of acetylcholine release via adenosine A1 receptor in rat cerebral cortex. Neurosci Lett 1996, 209:181-184.
79. Kurosawa M., Sato A., Sato Y. Stimulation of the nucleus basalis of Meynert increases acetylcholine release in the cerebral cortex in rats. Neurosci Lett 1989, 98:45-50.
80. Lamour Y., Dutar P., Jobert A. Cortical projections of the nucleus of the diagonal band of Broca and of the substantia innominata in the rat: an anatomical study using the anterograde transport of a conjugate of wheat germ agglutinin and horseradish peroxidase. Neuroscience 1984, 12:395-408.
81. Lamour Y., Dutar P., Rascol O., Jobert A. Basal forebrain neurons projecting to the rat frontoparietal cortex: electrophysiological and pharmacological properties. Brain Res 1986, 362:122-131.
82. Laplante F., Morin Y., Quirion R., Vaucher E. Acetylcholine release is elicited in the visual cortex, but not in the prefrontal cortex, by patterned visual stimulation: a dual in vivo microdialysis study with functional correlates in the rat brain. Neuroscience 2005, 132:501-510.
83. Laplante F., Srivastava L.K., Quirion R. Alterations in dopaminergic modulation of prefrontal cortical acetylcholine release in post-pubertal rats with neonatal ventral hippocampal lesions. J Neurochem 2004, 89:314-323.
84. Laplante F., Stevenson C.W., Gratton A., Srivastava L.K., Quirion R. Effects of neonatal ventral hippocampal lesion in rats on stress-induced acetylcholine release in the prefrontal cortex. J Neurochem 2004, 91:1473-1482.
85. Li Z., Huang M., Ichikawa J., Dai J., Meltzer H.Y. N-desmethylclozapine, a major metabolite of clozapine, increases cortical acetylcholine and dopamine release in vivo via stimulation of M1 muscarinic receptors. Neuropsychopharmacology 2005, 30:1986-1995.
86. Liang Y.Q., Huang X.T., Tang X.C. Huperzine A reverses cholinergic and monoaminergic dysfunction induced by bilateral nucleus basalis magnocellularis injection of beta-amyloid peptide (1-40) in rats. Cell Mol Neurobiol 2008, 28:87-101.
87. Lieberman J.A., Javitch J.A., Moore H. Cholinergic agonists as novel treatments for schizophrenia: the promise of rational drug development for psychiatry. Am J Psychiatry 2008, 165:931-936.
88. Losier B.J., Semba K. Dual projections of single cholinergic and aminergic brainstem neurons to the thalamus and basal forebrain in the rat. Brain Res 1993, 604:41-52.
89. Materi L.M., Rasmusson D.D., Semba K. Inhibition of synaptically evoked cortical acetylcholine release by adenosine: an in vivo microdialysis study in the rat. Neuroscience 2000, 97:219-226.
90. McGaughy J., Sandstrom M., Ruland S., Bruno J.P., Sarter M. Lack of effects of lesions of the dorsal noradrenergic bundle on behavioral vigilance. Behav Neurosci 1997, 111:646-652.
91. McGaughy J., Sarter M. Behavioral vigilance in rats: task validation and effects of age, amphetamine, and benzodiazepine receptor ligands. Psychopharmacology (Berl) 1995, 117:340-357.
92. Mesulam M. The cholinergic lesion of Alzheimer's disease: pivotal factor or side show?. Learn Mem 2004, 11:43-49.
93. Mesulam M.M., Geula C. Nucleus basalis (Ch4) and cortical cholinergic innervation in the human brain: observations based on the distribution of acetylcholinesterase and choline acetyltransferase. J Comp Neurol 1988, 275:216-240.
94. Mesulam M.M., Mufson E.J., Wainer B.H., Levey A.I. Central cholinergic pathways in the rat: an overview based on an alternative nomenclature (Ch1-Ch6). Neuroscience 1983, 10:1185-1201.
95. Metherate R., Cox C.L., Ashe J.H. Cellular bases of neocortical activation: modulation of neural oscillations by the nucleus basalis and endogenous acetylcholine. J Neurosci 1992, 12:4701-4711.
96. Mitchell K.M. Acetylcholine and choline amperometric enzyme sensors characterized in vitro and in vivo. Anal Chem 2004, 76:1098-1106.
97. Mogenson G.J., Swanson L.W., 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 1983, 3:189-202.
98. Moore H., Fadel J., Sarter M., Bruno J.P. Role of accumbens and cortical dopamine receptors in the regulation of cortical acetylcholine release. Neuroscience 1999, 88:811-822.
99. Moore H., Sarter M., Bruno J.P. Age-dependent modulation of in vivo cortical acetylcholine release by benzodiazepine receptor ligands. Brain Res 1992, 596:17-29.
100. Moore H., Sarter M., Bruno J.P. Bidirectional modulation of stimulated cortical acetylcholine release by benzodiazepine receptor ligands. Brain Res 1993, 627:267-274.
101. Moore H., Sarter M., Bruno J.P. Bidirectional modulation of cortical acetylcholine efflux by infusion of benzodiazepine receptor ligands into the basal forebrain. Neurosci Lett 1995, 189:31-34.
102. Moore H., Stuckman S., Sarter M., Bruno J.P. Stimulation of cortical acetylcholine efflux by FG 7142 measured with repeated microdialysis sampling. Synapse 1995, 21:324-331.
103. Moore H., Stuckman S., Sarter M., Bruno J.P. Potassium, but not atropine-stimulated cortical acetylcholine efflux, is reduced in aged rats. Neurobiol Aging 1996, 17:565-571.
104. Mufson E.J., Cochran E., Benzing W., Kordower J.H. Galaninergic innervation of the cholinergic vertical limb of the diagonal band (Ch2) and bed nucleus of the stria terminalis in aging, Alzheimer's disease and Down's syndrome. Dementia 1993, 4:237-250.
105. Mufson E.J., Deecher D.C., Basile M., Izenwasse S., Mash D.C. Galanin receptor plasticity within the nucleus basalis in early and late Alzheimer's disease: an in vitro autoradiographic analysis. Neuropharmacology 2000, 39:1404-1412.
106. Mufson E.J., Kahl U., Bowser R., Mash D.C., Kordower J.H., Deecher D.C. Galanin expression within the basal forebrain in Alzheimer's disease. Comments on therapeutic potential. Ann N Y Acad Sci 1998, 863:291-304.
107. Murrin L.C., DeHaven R.N., Kuhar M.J. On the relationship between (3H)choline uptake activation and (3H)acetylcholine release. J Neurochem 1977, 29:681-687.
108. Nair S.G., Gudelsky G.A. 3,4-Methylenedioxymethamphetamine enhances the release of acetylcholine in the prefrontal cortex and dorsal hippocampus of the rat. Psychopharmacology (Berl) 2006, 184:182-189.
109. Navera E.N., Sode K., Tamiya E., Karube I. Development of acetylcholine sensor using carbon fiber (amperometric determination). Biosens Bioelectron 1991, 6:675-680.
110. Nelson C.L., Burk J.A., Bruno J.P., Sarter M. Effects of acute and repeated systemic administration of ketamine on prefrontal acetylcholine release and sustained attention performance in rats. Psychopharmacology (Berl) 2002, 161:168-179.
111. Nelson C.L., Sarter M., Bruno J.P. Repeated pretreatment with amphetamine sensitizes increases in cortical acetylcholine release. Psychopharmacology (Berl) 2000, 151:406-415.
112. Nelson C.L., Sarter M., Bruno J.P. Prefrontal cortical modulation of acetylcholine release in posterior parietal cortex. Neuroscience 2005, 132:347-359.
113. Neubauer H., Adams M., Redfern P. The role of central cholinergic mechanisms in schizophrenia. Med Hypotheses 1975, 1:32-34.
114. Page K.J., Saha A., Everitt B.J. Differential activation and survival of basal forebrain neurons following infusions of excitatory amino acids: studies with the immediate early gene c-fos. Exp Brain Res 1993, 93:412-422.
115. Palmer A.M., DeKosky S.T. Monoamine neurons in aging and Alzheimer's disease. J Neural Transm Gen Sect 1993, 91:135-159.
116. Parikh V., Kozak R., Martinez V., Sarter M. Prefrontal acetylcholine release controls cue detection on multiple timescales. Neuron 2007, 56:141-154.
117. Pasumarthi R.K., Fadel J. Activation of orexin/hypocretin projections to basal forebrain and paraventricular thalamus by acute nicotine. Brain Res Bull 2008, 77:367-373.
118. Pepeu G., Giovannelli L., Casamenti F., Scali C., Bartolini L. Amyloid beta-peptides injection into the cholinergic nuclei: morphological, neurochemical and behavioral effects. Prog Brain Res 1996, 109:273-282.
119. Perry E.K. The cholinergic system in old age and Alzheimer's disease. Age Ageing 1980, 9:1-8.
120. Petkova-Kirova P., Rakovska A., Della Corte L., Zaekova G., Radomirov R., Mayer A. Neurotensin modulation of acetylcholine, GABA, and aspartate release from rat prefrontal cortex studied in vivo with microdialysis. Brain Res Bull 2008, 77:129-135.
121. Phillis J.W. Acetylcholine release from the central nervous system: a 50-year retrospective. Crit Rev Neurobiol 2005, 17:161-217.
122. Prus A.J., Huang M., Li Z., Dai J., Meltzer H.Y. The neurotensin analog NT69L enhances medial prefrontal cortical dopamine and acetylcholine efflux: potentiation of risperidone-, but not haloperidol-, induced dopamine efflux. Brain Res 2007, 1184:354-364.
123. Quirion R., Richard J., Wilson A. Muscarinic and nicotinic modulation of cortical acetylcholine release monitored by in vivo microdialysis in freely moving adult rats. Synapse 1994, 17:92-100.
124. Rasmusson D.D., Clow K., Szerb J.C. Frequency-dependent increase in cortical acetylcholine release evoked by stimulation of the nucleus basalis magnocellularis in the rat. Brain Res 1992, 594:150-154.
125. Rasmusson D.D., Szerb I.C., Jordan J.L. Differential effects of alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid and N-methyl-d-aspartate receptor antagonists applied to the basal forebrain on cortical acetylcholine release and electroencephalogram desynchronization. Neuroscience 1996, 72:419-427.
126. Richter D., Crossland J. Variation in acetylcholine content of the brain with physiological state. Am J Physiol 1949, 159:247-255.
127. Sahakian B.J., Owen A.M., Morant N.J., Eagger S.A., Boddington S., Crayton L., et al. Further analysis of the cognitive effects of tetrahydroaminoacridine (THA) in Alzheimer's disease: assessment of attentional and mnemonic function using CANTAB. Psychopharmacology (Berl) 1993, 110:395-401.
128. Sakurai T., Amemiya A., Ishii M., Matsuzaki I., Chemelli R.M., Tanaka H., et al. Orexins and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell 1998, 92:573-585.
129. Sarter M. Neuronal mechanisms of the attentional dysfunctions in senile dementia and schizophrenia: two sides of the same coin?. Psychopharmacology (Berl) 1994, 114:539-550.
130. Sarter M., Bruno J.P. Trans-synaptic stimulation of cortical acetylcholine and enhancement of attentional functions: a rational approach for the development of cognition enhancers. Behav Brain Res 1997, 83:7-14.
131. Sarter M., Nelson C.L., Bruno J.P. Cortical cholinergic transmission and cortical information processing in schizophrenia. Schizophr Bull 2005, 31:117-138.
132. Sarter M., Parikh V. Choline transporters, cholinergic transmission and cognition. Nat Rev Neurosci 2005, 6:48-56.
133. Sarter M., Parikh V., Howe W.M. Phasic acetylcholine release and the volume transmission hypothesis: time to move on. Nat Rev Neurosci 2009, 10:383-390.
134. Sarter M.F., Bruno J.P. Cognitive functions of cortical ACh: lessons from studies on trans-synaptic modulation of activated efflux. Trends Neurosci 1994, 17:217-221.
135. Scali C., Casamenti F., Pazzagli M., Bartolini L., Pepeu G. Nerve growth factor increases extracellular acetylcholine levels in the parietal cortex and hippocampus of aged rats and restores object recognition. Neurosci Lett 1994, 170:117-120.
136. Scali C., Giovannini M.G., Prosperi C., Bartolini L., Pepeu G. Tacrine administration enhances extracellular acetylcholine in vivo and restores the cognitive impairment in aged rats. Pharmacol Res 1997, 36:463-469.
137. Scatton B., Bartholini G. gamma-Aminobutyric acid (GABA) receptor stimulation. IV. Effect of progabide (SL 76002) and other GABAergic agents on acetylcholine turnover in rat brain areas. J Pharmacol Exp Ther 1982, 220:689-695.
138. Schuvailo O.N., Dzyadevych S.V., El'skaya A.V., Gautier-Sauvigne S., Csoregi E., Cespuglio R., et al. Carbon fibre-based microbiosensors for in vivo measurements of acetylcholine and choline. Biosens Bioelectron 2005, 21:87-94.
139. Seguela P., Watkins K.C., Geffard M., Descarries L. Noradrenaline axon terminals in adult rat neocortex: an immunocytochemical analysis in serial thin sections. Neuroscience 1990, 35:249-264.
140. Semba K., Reiner P.B., McGeer E.G., Fibiger H.C. Brainstem afferents to the magnocellular basal forebrain studied by axonal transport, immunohistochemistry, and electrophysiology in the rat. J Comp Neurol 1988, 267:433-453.
141. Sim J.A., Griffith W.H. Muscarinic inhibition of glutamatergic transmissions onto rat magnocellular basal forebrain neurons in a thin-slice preparation. Eur J Neurosci 1996, 8:880-891.
142. Smiley J.F., Mesulam M.M. Cholinergic neurons of the nucleus basalis of Meynert receive cholinergic, catecholaminergic and GABAergic synapses: an electron microscopic investigation in the monkey. Neuroscience 1999, 88:241-255.
143. Smiley J.F., Subramanian M., Mesulam M.M. Monoaminergic-cholinergic interactions in the primate basal forebrain. Neuroscience 1999, 93:817-829.
144. Smith C.G., Beninger R.J., Mallet P.E., Jhamandas K., 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 1994, 666:61-67.
145. Struble R.G., Lehmann J., Mitchell S.J., McKinney M., Price D.L., Coyle J.T., et al. Basal forebrain neurons provide major cholinergic innervation of primate neocortex. Neurosci Lett 1986, 66:215-220.
146. Summers K.L., Giacobini E. Effects of local and repeated systemic administration of (-)nicotine on extracellular levels of acetylcholine, norepinephrine, dopamine, and serotonin in rat cortex. Neurochem Res 1995, 20:753-759.
147. Szerb J.C., Clow K., Rasmusson D.D. Pharmacological but not physiological modulation of cortical acetylcholine release by cholinergic mechanisms in the nucleus basalis magnocellularis. Can J Physiol Pharmacol 1994, 72:893-898.
148. Tandon R., Greden J.F. Cholinergic hyperactivity and negative schizophrenic symptoms. A model of cholinergic/dopaminergic interactions in schizophrenia. Arch Gen Psychiatry 1989, 46:745-753.
149. Tang Y., Aigner T.G. Release of cerebral acetylcholine increases during visually mediated behavior in monkeys. Neuroreport 1996, 7:2231-2235.
150. Tani Y., Saito K., Imoto M., Ohno T. Pharmacological characterization of nicotinic receptor-mediated acetylcholine release in rat brain-an in vivo microdialysis study. Eur J Pharmacol 1998, 351:181-188.
151. Toide K., Iwamoto Y., Fujiwara T., Abe H. JTP-4819: a novel prolyl endopeptidase inhibitor with potential as a cognitive enhancer. J Pharmacol Exp Ther 1995, 274:1370-1378.
152. Toide K., Shinoda M., Iwamoto Y., Fujiwara T., Okamiya K., Uemura A. A novel prolyl endopeptidase inhibitor, JTP-4819, with potential for treating Alzheimer's disease. Behav Brain Res 1997, 83:147-151.
153. Toide K., Shinoda M., Takase M., Iwata K., Yoshida H. Effects of a novel thyrotropin-releasing hormone analogue, JTP-2942, on extracellular acetylcholine and choline levels in the rat frontal cortex and hippocampus. Eur J Pharmacol 1993, 233:21-28.
154. Van Dort C.J., Baghdoyan H.A., Lydic R. Adenosine A(1) and A(2A) receptors in mouse prefrontal cortex modulate acetylcholine release and behavioral arousal. J Neurosci 2009, 29:871-881.
155. Wainer B.H., Steininger T.L., Roback J.D., Burke-Watson M.A., Mufson E.J., Kordower J. Ascending cholinergic pathways: functional organization and implications for disease models. Prog Brain Res 1993, 98:9-30.
156. Wang H.Y., Wild K.D., Shank R.P., Lee D.H. Galanin inhibits acetylcholine release from rat cerebral cortex via a pertussis toxin-sensitive G(i)protein. Neuropeptides 1999, 33:197-205.
157. Wang X.C., Du X.X., Tian Q., Wang J.Z. Correlation between choline signal intensity and acetylcholine level in different brain regions of rat. Neurochem Res 2008, 33:814-819.
158. Weiss J.H., Yin H.Z., Choi D.W. Basal forebrain cholinergic neurons are selectively vulnerable to AMPA/kainate receptor-mediated neurotoxicity. Neuroscience 1994, 60:659-664.
159. Wenk G., Hepler D., Olton D. Behavior alters the uptake of [3H]choline into acetylcholinergic neurons of the nucleus basalis magnocellularis and medial septal area. Behav Brain Res 1984, 13:129-138.
160. Wenk G.L. Pharmacological manipulations of the substantia innominata-cortical cholinergic pathway. Neurosci Lett 1984, 51:99-103.
161. 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 1982, 215:1237-1239.
162. Wu C.F., Bertorelli R., Sacconi M., Pepeu G., Consolo S. Decrease of brain acetylcholine release in aging freely-moving rats detected by microdialysis. Neurobiol Aging 1988, 9:357-361.
163. Zaborszky L. Afferent connections of the forebrain cholinergic projection neurons, with special reference to monoaminergic and peptidergic fibers. Exs 1989, 57:12-32.
164. Zaborszky L. The modular organization of brain systems. Basal forebrain: the last frontier. Prog Brain Res 2002, 136:359-372.
165. Zaborszky L., Cullinan W.E. Hypothalamic axons terminate on forebrain cholinergic neurons: an ultrastructural double-labeling study using PHA-L tracing and ChAT immunocytochemistry. Brain Res 1989, 479:177-184.
166. Zaborszky L., 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 1992, 570:92-101.
167. Zaborszky L., Gaykema R.P., Swanson D.J., Cullinan W.E. Cortical input to the basal forebrain. Neuroscience 1997, 79:1051-1078.
168. Zmarowski A., Sarter M., Bruno J.P. Glutamate receptors in nucleus accumbens mediate regionally selective increases in cortical acetylcholine release. Synapse 2007, 61:115-123.