The role of acetylcholine in cortical synaptic plasticity

Behavioural Brain Research

Volumn 115, Issue 2, 2000, Pages 205-218

  Rasmusson, D D ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

Author keywords

Cholinergic; Cortex; Hippocampus; Muscarinic; Nicotinic; Sensory

Indexed keywords

ACETYLCHOLINE;

BRAIN CORTEX; CHOLINERGIC SYSTEM; ELECTROSTIMULATION; FACILITATION; FOREBRAIN; IN VITRO STUDY; IN VIVO STUDY; MICROIONTOPHORESIS; NEOCORTEX; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NERVE POTENTIAL; NONHUMAN; OLFACTORY CORTEX; PRIORITY JOURNAL; REVIEW;

EID: 0033800404     PISSN: 01664328     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0166-4328(00)00259-X     Document Type: Article

References (159)

1. Abe K., Nakata A., Mizutani A., Saito H. Facilitatory but nonessential role of muscarinic cholinergic system in the generation of long-term potentiation of population spikes in the dendritic gyrus in vivo. Neuropharmacology. 33:1994;847-852.
2. Adams C.E., Cepeda C., Boylan M.K., Fisher R.S., Hull C.D., Buchwald N.A., Wainer B.H., Levine M.S. Basal forebrain neurons have axon collaterals that project to widely divergent cortical areas in the cat. Brain Res. 397:1986;365-371.
3. Adams R.W., Lambert G.A., Lance J.W. Brain-stem facilitation of electrically evoked visual cortical responses in the cat. Source, pathway and role of nicotinic receptors. Electroencephalogr. Clin. Neurophysiol. 69:1988;45-54.
4. Akaishi T., Kimura A., Sato A., Suzuki A. Responses of neurons in the nucleus basalis of Meynert to various afferent stimuli in rats. Neuroreport. 1:1990;37-39.
5. Andrade R. Cell excitation enhances muscarinic cholinergic responses in rat association cortex. Brain Res. 548:1991;81-93.
6. Aoki C., Kabak S. Cholinergic terminals in the cat visual cortex: Ultrastructural basis for interaction with glutamate-immunoreactive neurons and other cells. Vis. Neurosci. 8:1992;177-191.
7. Armstrong-James M., Diamond M.E., Ebner F.F. An innocuous bias in whisker use in adult rats modifies receptive fields of barrel cortex neurons. J. Neurosci. 14:1994;6978-6991.
8. Ashe J.H., McKenna T.M., Weinberger N.M. Cholinergic modulation of frequency receptive fields in auditory cortex: II. Frequency-specific effects of anticholinesterases provide evidence for a modulatory action of endogenous ACh. Synapse. 4:1989;44-54.
9. Aston-Jones G., Shaver R., Dinan T.G. Nucleus basalis neurons exhibit axonal branching with decreased impulse conduction velocity in rat cerebrocortex. Brain Res. 325:1985;271-285.
10. Auerbach J.M., Segal M. Muscarinic receptors mediating depression and long-term potentiation in rat hippocampus. J. Physiol. 492:1996;479-493.
11. Auerbach J.M., Segal M. A novel cholinergic induction of long-term potentiation in rat hippocampus. J. Neurophysiol. 72:1994;2034-2040.
12. Bakin J.S., Weinberger N.M. Induction of a physiological memory in the cerebral cortex by stimulation of the nucleus basalis. Proc. Natl. Acad. Sci. USA. 93:1996;11219-11224.
13. Baskerville K.A., Chang H.T., Herron P. Topography of cholinergic afferents from the nucleus basalis of Meynert to representational areas of sensorimotor cortices in the rat. J. Comp. Neurol. 335:1993;552-562.
14. Baskerville K.A., Schweitzer J.B., Herron P. Effects of cholinergic depletion on experience-dependent plasticity in the cortex of the rat. Neuroscience. 80:1997;1159-1169.
15. Bear M.F., Singer W. Modulation of visual cortical plasticity by acetylcholine and noradrenaline. Nature. 320:1986;172-176.
16. Bernardo L.S., Prince D.A. Cholinergic excitation of mammalian hippocampal pyramidal cells. Brain Res. 249:1982;315-331.
17. 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. 8:1982;727-749.
18. 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. Behav. Neurosci. 112:1998;467-479.
19. Blitzer R.D., Gil O., Landau E.M. Cholinergic stimulation enhances long-term potentiation in the CA1 region of rat hippocampus. Neurosci. Lett. 119:1990;207-210.
20. Blokland A. Acetylcholine: a neurotransmitter for learning and memory? Brain Res. Rev. 21:1996;285-300.
21. Boylan M.K., Fisher R.S., Hull C.D., Buchwald N.A., Levine M.S. Axonal branching of basal forebrain projections to the neocortex: a double-labelling study in the cat. Brain Res. 375:1986;176-181.
22. Bröcher S., Artola A., Singer W. Agonists of cholinergic and noradrenergic receptors facilitate synergistically the induction of long-term potentiation in slices of rat visual cortex. Brain Res. 573:1992;27-36.
23. Broide R.S., Leslie F.M. The alpha7 nicotinic acetylcohline receptor in neuronal plasticity. Mol. Neurobiol. 20:1999;1-16.
24. Burgard E.C., Sarvey J.M. Muscarinic receptor activation facilitates the induction of long-term potentiation (LTP) in the rat dentate gyrus. Neurosci. Lett. 116:1990;34-39.
25. Casamenti F., Deffenu G., Abbamondi A.L., Pepeu G. Changes in cortical acetylcholine output induced by modulation of the nucleus basal. Brain Res. Bull. 16:1986;689-695.
26. Celesia G.G., Jasper H.H. Acetylcholine released from cerebral cortex in relation to state of activation. Neurology. 16:1966;1053-1064.
27. Chrobak J.J., Hanin I., Schmechel D.E., Walsh T.J. AF64A-induced working memory impairment: behavioral, neurochemical and histological correlates. Brain Res. 463:1988;107-117.
28. Cole A.E., Nicoll R.A. Characterization of a slow cholinergic post-synaptic potential recorded in vitro from rat hippocampal pyramidal cells. J. Physiol. 352:1984;173-188.
29. Collier B., Mitchell J.F. The central release of acetylcholine during stimulation of the visual pathway. J. Physiol. 184:1966;239-254.
30. Delacour J., Houcine O., Costa J.C. Evidence for a cholinergic mechanism of 'learned' changes in the responses of barrel field neurons of the awake and undrugged rat. Neurosci. 34:1990;1-8.
31. Delacour J., Houcine O., Talbi B. Learned changes in the responses of the rat barrel field neurons. Neuroscience. 23:1987;63-71.
32. Détári L., Rasmusson D.D., Semba K. Phasic relationship between the activity of basal forebrain neurons and cortical EEG in urethane-anesthetized rat. Brain Res. 759:1997;112-121.
33. Détári L., Semba K., Rasmusson D.D. Responses of cortical EEG-related basal forebrain neurons to brainstem and sensory stimulation in urethane-anesthetized rat. Eur. J. Neurosci. 9:1997;1153-1161.
34. Détári L., Vanderwolf C.H. Activity of identified cortically projecting and other basal forebrain neurones during large slow waves and cortical activation in anaesthetized rats. Brain Res. 437:1987;1-8.
35. Diamond M.E., Armstrong-James M., Ebner F.F. Experience-dependent plasticity in adult rat barrel cortex. Proc. Natl. Acad. Sci. USA. 90:1993;2082-2086.
36. Dimyan M.A., Weinberger N.M. Basal forebrain stimulation induces discriminative receptive field plasticity in the auditory cortex. Behav. Neurosci. 113:1999;691-702.
37. Donoghue J.P., Carroll K.L. Cholinergic modulation of sensory responses in rat primary somatic sensory cortex. Brain Res. 408:1987;367-371.
38. Dudar J.D. The effect of septal nuclei stimulation on the release of acetylcholine from the rabbit hippocampus. Brain Res. 83:1975;123-133.
39. Dunnett S.B., Whishaw I.Q., Jones G.H., Bunch S.T. Behavioral, biochemical and histochemical effects of different neurotoxic amino acids injected into nucleus basal magnocellularis of rats. Neuroscience. 20:1987;653-669.
40. Dykes R.W. Acetylcholine and neuronal plasticity in somatosensory cortex. Steriade M., Biesold D. Brain Cholinergic Systems. 1990;294-313 Oxford University Press, Oxford, UK.
41. Edeline J.-M. Learning-induced physiological plasticity in the thalamo-cortical sensory systems: a critical evaluation of receptive field plasticity, map changes and their potential mechanisms. Prog. Neurobiol. 57:1999;165-234.
42. Edeline J.-M., Hars B., Maho C., Hennevin E. Transient and prolonged facilitation of tone-evoked responses induced by basal forebrain stimulations in the rat auditory cortex. Exp. Brain Res. 97:1994;373-386.
43. Edwards F.A. Anatomy and electrophysiology of fast central synapses lead to a structural model for long-term potentiation. Physiol. Rev. 75:1995;759-787.
44. Giovannini M.G., Bartolini L., Kopf S.R., Pepeu G. Acetylcholine release from the frontal cortex during exploratory activity. Brain Res. 784:1998;218-227.
45. Giovannini M.G., Camilli F., Mundula A., Pepeu G. Glutamatergic regulation of acetylcholine output in different brain regions: a microdialysis study in the rat. Neurochem. Int. 25:1994;23-26.
46. Giovannini M.G., Mutolo D., Bianchi L., Michelassi A., 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.
47. Gordon B., Mitchell B., Mohtadi K., Roth E., Tseng Y., Turk F. Lesions of nonvisual inputs affect plasticity, norepinephrine content, and acetylcholine content of visual cortex. J. Neurophysiol. 64:1990;1851-1860.
48. Gray R., Rajan A.S., Radcliffe K.A., Yakehiro M., Dani J.A. Hippocampal synaptic transmission enhanced by low concentrations of nicotine [see comments]. Nature. 383:1996;713-716.
49. Gritti I., Mainville L., Mancia M., Jones B.E. GABAergic and other noncholinergic basal forebrain neurons, together with cholinergic neurons, project to the mesocortex and isocortex in the rat. J. Comp. Neurol. 383:1997;163-177.
50. Gu Q., Singer W. Effects of intracortical infusion of anticholinergic drugs on neuronal plasticity in kitten striate cortex. Eur. J. Neurosci. 5:1993;475-485.
51. Halliwell J.V., Adams P.R. Voltage-clamp analysis of muscarinic excitaiton in hippocampal neurons. Brain Res. 250:1982;71-92.
52. Hanin I. The AF64A model of cholinergic hypofunction: an update. Life Sci. 58:1996;1955-1964.
53. Hars B., Maho C., Edeline J.-M., Hennevin E. Basal forebrain stimulation facilitates tone-evoked responses in the auditory cortex of awake rat. Neuroscience. 56:1993;61-76.
54. Hashimoto T., Shu H., Kuriyama K. Muscarinic M1 receptor mediated inhibition of GABA release from rat cerebral cortex. Neurochem. Int. 24:1994;389-394.
55. Hasselmo M.E., Anderson B.P., Bower J.M. Cholinergic modulation of cortical associative memory function. J. Neurophysiol. 67:1992;1230-1246.
56. Hasselmo M.E., Barkai E. Cholinergic modulation of activity-dependent synaptic plasticity in the piriform cortex and associative memory function in a network biophysical simulation. J. Neurosci. 15:1995;6592-6604.
57. Hasselmo M.E., Bower J.M. Cholinergic suppression specific to intrinsic not afferent fiber synapses in rat piriform (olfactory) cortex. J. Neurophysiol. 67:1992;1222-1229.
58. Hemsworth B.A., Mitchell J.F. The characteristics of acetylcholine release mechanisms in the auditory cortex. Brit. J. Pharmacol. 36:1969;161-170.
59. Hess G., Donoghue J.P. Facilitation of long-term potentiation in layer II/III horizontal connections of rat motor cortex following layer I stimulation: route of effect and cholinergic contributions. Exp. Brain Res. 127:1999;279-290.
60. 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. 86:1998;949-957.
61. Hirotsu I., Hori N., Katsuda N., Ishihara T. Effect of anticholinergic drug on long-term potentiation in rat hippocampal slices. Brain Res. 482:1989;194-197.
62. Höhmann C.F., Brooks A.R., Coyle J.T. Neonatal lesions of the basal forebrain cholinergic neurons result in abnormal cortical development. Dev. Brain Res. 42:1988;253-264.
63. Howard M.A., Simons D.J. Physiologic effects of nucleus basalis magnocellularis stimulation on rat barrel cortex neurons. Exp. Brain Res. 102:1994;21-33.
64. Jacobs S., Code R., Juliano S. Basal forebrain lesions alter stimulus-evoked metabolic activity in rat somatosensory cortex. Brain Res. 560:1991;342-345.
65. Jiménez-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. 71:1996;5677-5679.
66. Jiménez-Capdeville M.E., Dykes R.W. Daily changes in the release of acetylcholine from rat primary somatosensory cortex. Brain Res. 625:1993;152-158.
67. Jiménez-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. 381:1997;53-67.
68. Jouvenceau A., Billard J.M., Lamour Y., Dutar P. Persistence of CA1 hippocampal LTP after selective cholinergic denervation. Neuroreport. 7:1996;948-952.
69. Juliano S., Ma W., Eslin D. Cholinergic depletion prevents expansion of topographic maps in somatosensory cortex. Proc. Natl. Acad. Sci. USA. 88:1991;780-784.
70. Juliano S.L., Ma W., Bear M.F., Eslin D. Cholinergic manipulation alters stimulus-evoked metabolic activity in cat somatosensory cortex. J. Comp. Neurol. 297:1990;106-120.
71. Juliano S.L., Whitsel B.L. A combined 2-deoxyglucose and neurophysiological study of primate somatosensory cortex. J. Comp. Neurol. 263:1987;514-525.
72. Kaas J. Plasticity of sensory and motor maps in adult mammals. Annu. Rev. Neurosci. 14:1991;137-167.
73. Kanai T., Szerb J.C. Mesencephalic reticular activating system and cortical acetylcholine output. Nature. 205:1965;80-82.
74. Kaneko S., Maeda T., Satoh M. Cognitive enhancers and hippocampal long-term potentiation in vitro. Behav. Brain Res. 83:1997;45-49.
75. Khateb A., Fort P., Williams S., Serafin M., Mühlethaler M., Jones B.E. GABAergic input to cholinergic nucleus basalis neurons. Neuroscience. 86:1998;937-947.
76. Kilgard M.P., Merzenich M.M. Cortical map reorganization enabled by nucleus basalis activity. Science. 279:1998;1714-1718.
77. Kirkwood A., Rozas C., Kirkwood J., Perez F., Bear M.F. Modulation of long-term synaptic depression in visual cortex by acetylcholine and norepinephrine. J. Neurosci. 19:1999;1599-1609.
78. Krnjevic K., Phillis J.W. Acetylcholine-sensitive cells in the cerebral cortex. J. Physiol. 166:1963;296-327.
79. Krnjevic K., Pumain R., Renaud L. The mechanism of excitation by acetylcholine in the cerebral cortex. J. Physiol. 215:1971;247-268.
80. Krnjevic K., Ropert N. Electrophysiological and pharmacological characteristics of facilitation of hippocampal population spikes by stimulation of the medial septum. Neuroscience. 7:1982;2165-2183.
81. Kurosawa M., Sato A., Sato Y. Cutaneous mechanical sensory stimulation increases extracellular acetylcholine release in cerebral cortex in anesthetized rats. Neurochem. Int. 21:1992;423-427.
82. Kurosawa M., Sato A., Sato Y. Stimulation of the nucleus basalis of Meynert increases acetylcholine release in the cerebral cortex in rats. Neurosci. Lett. 98:1989;45-50.
83. Lamour Y., Dutar P., Jobert A., Dykes R.W. An iontophoretic study of single somatosensory neurons in rat granular cortex serving the limbs: a laminar analysis of glutamate and acetylcholine effects on receptive-field properties. J. Neurophysiol. 60:1988;725-750.
84. Lamour Y., Senut M.C., Bassant M.H., Dutar P. Functional properties of septo-hippocampal neurons. Steriade M., Biesold D. Brain Cholinergic Systems. 1990;265-281 Oxford University Press, Oxford, UK.
85. Lewandowski M.H., Müller C.M., Singer W. Reticular facilitation of cat visual cortical responses is mediated by nicotinic and muscarinic cholinergic mechanisms. Exp. Brain Res. 96:1993;1-7.
86. Lin Y., Phillis J.W. Muscarinic agonist-mediated induction of long-term potentiation in rat cerebral cortex. Brain Res. 551:1991;342-345.
87. Linster C., Wyble B.P., Hasselmo M.E. Electrical stimulation of the horizontal limb of the diagonal band of Broca modulates population EPSPs in piriform cortex. J. Neurophysiol. 81:1999;2737-2742.
88. Lorens S.A., Kindel G., Dong X.W., Lee J.M., Hanin I. Septal choline acetyltransferase immunoreactive neurons: dose-dependent effects of AF64A. Brain Res. Bull. 26:1991;965-971.
89. Ma W., Höhmann C.F., Coyle J.T., Juliano S.L. Lesions of the basal forebrain alter stimulus-evoked metabolic activity in mouse somatosensory cortex. J. Comp. Neurol. 288:1989;414-427.
90. Maalouf M., Miasnikov A.A., Dykes R.W. Blockade of cholinergic receptors in rat barrel cortex prevents long-term changes in the evoked potential during sensory preconditioning. J. Neurophysiol. 80:1998;529-545.
91. Maeda T., Kaneko S., Satoh M. Roles of endogenous cholinergic neurons in the induction of long-term potentiation at hippocampal mossy fiber synapses. Neurosci. Res. 20:1994;71-78.
92. Malenka R.C., Nicoll R.A. Long-term potentiation - a decade of progress? Science. 285:1999;1870-1874.
93. Markram H., Segal M. Long-lasting facilitation of excitatory postsynaptic potentials in the rat hippocampus by acetylcholine. J. Physiol. 427:1990;381-393.
94. Mash D.C., Potter L.T. Autoradiographic localization of M1 and M2 muscarine receptors in the rat brain. Neuroscience. 19:1986;551-564.
95. McCormick D.A., Prince D.A. Mechanisms of action of acetylcholine in the guinea-pig cerebral cortex in vitro. J. Physiol. London. 375:1986;169-194.
96. McKenna T.M., Ashe J.H., Hui G.K., Weinberger N.M. Muscarinic agonists modulate spontaneous and evoked unit discharge in auditory cortex of cat. Synapse. 2:1988;54-68.
97. McKenna T.M., Ashe J.H., Weinberger N.M. Cholinergic modulation of frequency receptive fields in auditory cortex: I. Frequency-specific effects of muscarinic agonists. Synapse. 4:1989;30-43.
98. Metherate R., Ashe J. Basal forebrain stimulation modifies auditory cortex responsiveness by an action at muscarinic receptors. Brain Res. 559:1991;163-167.
99. Metherate R., Ashe J.H. Nucleus basalis stimulation facilitates thalamocortical synaptic transmission in the rat auditory cortex. Synapse. 14:1993;132-143.
100. Metherate R., Tremblay N., Dykes R.W. Acetylcholine permits long-term enhancement of neuronal responsiveness in cat primary somatosensory cortex. Neuroscience. 22:1987;75-81.
101. Metherate R., Tremblay N., Dykes R.W. Transient and prolonged effects of acetylcholine on responsiveness of cat somatosensory cortical neurons. J. Neurophysiol. 59:1988;1253-1276.
102. Metherate R., Weinberger N.M. Acetylcholine produces stimulus-specific receptive field alterations in cat auditory cortex. Brain Res. 480:1989;372-377.
103. Metherate R., Weinberger N.M. Cholinergic modulation of responses to single tones produces tone-specific receptive field alterations in cat auditory cortex. Synapse. 6:1990;133-145.
104. 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. 3:1983;189-202.
105. Moor E., Auth F., DeBoer P., Westerink B.H.C. Septal and hippocampal glutamate receptors modulate the output of acetylcholine in hippocampus: a microdialysis study. J. Neurochem. 67:1996;310-316.
106. 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. 189:1995;31-34.
107. Müller C.M., Singer W. Acetylcholine-induced inhibition in the cat visual cortex is mediated by a GABAergic mechanism. Brain Res. 487:1989;335-342.
108. Mullin W.J. The effect of graded forelimb afferent volleys on acetylcholine release from cat sensorimotor cortex. J. Physiol. 244:1975;741-756.
109. Murphy P.C., Sillito A.M. Cholinergic enhancement of direction selectivity in the visual cortex of the cat. Neuroscience. 40:1991;13-20.
110. Neal M.J., Hemsworth B.A., Mitchell J.F. The excitation of central cholinergic mechanisms by stimulation of the auditory pathway. Life Sci. 7:1968;757-763.
111. Nuñez A. Unit activity of rat basal forebrain neurons: Relationship to cortical activity. Neuroscience. 72:1996;757-766.
112. Patil M.M., Hasselmo M.E. Modulation of inhibitory synaptic potentials in the piriform cortex. J. Neurophysiol. 81:1999;2103-2118.
113. Patil M.M., Linster C., Lubenov E., Hasselmo M.E. Cholinergic agonist carbachol enables associative long-term potentiation in piriform cortex slices. J. Neurophysiol. 80:1998;2467-2474.
114. Phillis J.W. Acetylcholine release from the cerebral cortex: its role in cortical arousal. Brain Res. 7:1968;378-389.
115. Phillis J.W., York D.H. Pharmacological studies on a cholinergic inhibition in the cerebral cortex. Brain Res. 10:1968;297-306.
116. Pirch J., Rigdon G., Rucker H., Turco K. Basal forebrain modulation of cortical cell .Activity during conditioning. Napier T.C., Kalivas P.W., Hanin I. The Basal Forebrain. Anatomy to Function. 1991;219-231 Plenum, New York.
117. Pitler T.A., Alger B.E. Cholinergic excitation of GABAergic interneurons int he rat hippocampal slice. J. Physiol. 450:1992;127-142.
118. Porter J.T., Cauli B., Tsuzuki K., Lambolez B., Rossier J., Audinat E. Selective excitation of subtypes of neocortical interneurons by nicotinic receptors. J. Neurosci. 19:1999;5228-5235.
119. Price J.L., Stern R. Individual cells in the nucleus basalis-diagonal band complex have restricted axonal projections to the cerebral cortex in the rat. Brain Res. 269:1983;352-356.
120. Rasmusson D., Szerb J.C. Acetylcholine release from visual and sensorimotor cortices of conditioned rabbits: the effects of sensory cuing and patterns of responding. Brain Res. 104:1976;243-259.
121. Rasmusson D.D. Cholinergic modulation of sensory information. Prog. Brain Res. 98:1993;357-364.
122. 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. 594:1992;150-154.
123. Rasmusson D.D., Clow K., Szerb J.C. Modification of neocortical acetylcholine release and EEG desynchronization due to brainstem stimulation by drugs applied to the basal forebrain. Neuroscience. 60:1994;665-677.
124. Rasmusson D.D., Dykes R.W. Long-term enhancement of evoked potentials in cat somatosensory cortex produced by co-activation of the basal forebrain and cutaneous receptors. Exp. Brain Res. 70:1988;276-286.
125. Richardson R.T., DeLong M.R. Functional implications of tonic and phasic activity changes in nucleus basalis neurons. Richardson R.T. Activation to Acquisition: Functional Aspects of the Basal Forebrain Cholinergic Systems. 1991;135-166 Birkhäuser, Boston.
126. Richardson R.T., DeLong M.R. Nucleus basalis of Meynert neuronal activity during a delayed response task in monkey. Brain Res. 399:1986;364-368.
127. Sachdev R.N.S., Lu S.-M., Wiley R.G., Ebner F.F. Role of the basal forebrain cholinergic projection in somatosensory cortical plasticity. J. Neurophysiol. 79:1998;3216-3228.
128. Saper C.B. Organization of cerebral cortical afferent systems in the rat. I. Magnocellular basal nucleus. J. Comp. Neurol. 222:1984;313-342.
129. Sarter M., Bruno J.P. Cognitive functions of cortical acetylcholine: toward a unifying hypothesis. Brain Res. Rev. 23:1997;28-46.
130. Sarter M., Dudchenko P. Dissociative effects of ibotenic and quisqualic acid-induced basal forebrain lesions on cortical acetylcholinesterase-positive fiber density and cytochrome oxidase activity. Neuroscience. 41:1991;729-738.
131. Sato H., Hata Y., Hagihara K., Tsumoto T. Effects of cholinergic depletion on neuron activities in the cat visual cortex. J. Neurophysiol. 58:1987;781-794.
132. Sato H., Hata Y., Masui H., Tsumoto T. A functional role of cholinergic innervation to neurons in the cat visual cortex. J. Neurophysiol. 58:1987;765-780.
133. Schliebs R., Roßner S., Bigl V. Immunolesion by 192IgG-saporin of rat basal forebrain cholinergic system: a useful tool to produce cortical cholinergic dysfunction. Klein J., Löffelholz K. Programme of Brain Research. 109:1996;253-264 Elsevier, Amsterdam.
134. Semba K., Fibiger H.C. Organization of central cholinergic systems. Nordberg A., Fuxe K., Holmstedt B., Sundwall A. Programme of Brain Research. 79:1989;37-63 Elsevier, Amsterdam.
135. Sillito A.M., Kemp J.A. Cholinergic modulation of the functional organization of the cat visual cortex. Brain Res. 289:1983;143-155.
136. Singer W. Central-core control of visual-cortex functions. Schmitt F.O., Worden F.G. Neurosciences: Fourth Study Program. 1979;1093-1110 MIT Press, Cambridge, MA.
137. Singer W. Role of acetylcholine in use-dependent plasticity of the visual cortex. Steriade M., Biesold D. Brain Cholinergic Systems. 1990;314-336 Oxford University Press, Oxford, UK.
138. Smith C.M. Acetylcholine release from the cholinergic septo-hippocampal pathway. Life Sci. 14:1974;2159-2166.
139. Spehlmann R. Acetylcholine and prostigmine electrophoresis at visual cortex neurons. J. Neurophysiol. 26:1963;127-139.
140. Stichel C.C., Singer W. Quantitative analysis of the choline acetyltransferase-immunoreactive axonal network in the cat primary visual cortex: I. adult cats. J. Comp. Neurol. 258:1987;91-98.
141. Stone T.W. Cholinergic mechanisms in the rat somatosensory cerebral cortex. J. Physiol. 225:1972;485-499.
142. Tremblay N., Warren R.A., 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.
143. Tremblay N., Warren R.A., Dykes R.W. Electrophysiological studies of acetylcholine and the role of the basal forebrain in the somatosensory cortex of the cat. I. Cortical neurons excited by glutamate. J. Neurophysiol. 64:1990;1199-1211.
144. Vanderwolf C.H., Cain D.P. The behavioral neurobiology of learning and memory: a conceptual reorientation. Brain Res. Rev. 19:1994;264-297.
145. Vidal C., Changeux J.-P. Nicotinic and muscarinic modulations of excitatory synaptic transmission in the rat prefrontal cortex in vitro. Neuroscience. 56:1993;23-32.
146. Wainer B.H., Mesulam M.-M. Ascending cholinergic pathways in the rat brain. Steriade M., Biesold D. Brain Cholinergic Systems. 1990;65-119 Oxford University Press, Oxford, UK.
147. Webster H.H., Hanisch U.-K., Dykes R.W., Biesold D. Basal forebrain lesions with or without reserpine injection inhibit cortical reorganization in rat hindpaw primary somatosensory cortex following sciatic nerve section. Somatosens. Motor Res. 8:1991;327-346.
148. Webster H.H., Rasmusson D.D., Dykes R.W., Schliebs R., Schober W., Brückner G., Biesold D. Long-term enhancement of evoked potentials in raccoon somatosensory cortex following co-activation of the nucleus basal of Meynert complex and cutaneous receptors. Brain Res. 545:1991;292-296.
149. Wenk G.L. The nucleus basalis magnocellularis cholinergic system: one hundred years of progress. Neurobiol. Learn. Mem. 67:1997;85-95.
150. Wenk G.L., Harrington C.A., Tucker D.A., Rance N.E., Walker L.C. Basal forebrain neurons and memory: A biochemical, histological, and behavioral study of differential vulnerability to ibotenate and quisqualate. Beh. Neurosci. 106:1992;909-923.
151. Wiesel T., Hubel D.H. Single-cell response in striate cortex of kittens deprived of vision in one eye. J. Neurophysiol. 26:1963;1003-1017.
152. Wiley R.G. Neural lesioning with ribosome-inactivating proteins: suicide transport and immunolesioning. Trends Neurosci. 15:1992;285-290.
153. Williams S., Johnston D. Muscarinic depression of long-term potentiation in CA3 hippocampal neurons. Science. 242:1988;84-87.
154. Woody C.D., Swartz B.E., Gruen E. Effects of acetylcholine and cyclic GMP on input resistance of cortical neurons in awake cats. Brain Res. 158:1978;373-395.
155. Xiang Z., Huguenard J.R., Prince D.A. Cholinergic switching within neocortical inhibitory networks. Science. 281:1998;985-988.
156. Záborszky L., Heimer L., Eckenstein F., Lertanth C. GABAergic input to cholinergic forebrain neurons: an ultrastructural study using retrograde tracing of HRP and double immunolabeling. J. Comp. Neurol. 250:1986;282-295.
157. Záborszky L., Pang K., Somogyi J., Nadasdy Z., Kallo I. The basal forebrain corticopetal system revisited. Ann. NY Acad. Sci. 877:1999;339-367.
158. Zhu X.O., Waite P.M.E. Cholinergic depletion reduces plasticity of barrel field cortex. Cerebral Cortex. 8:1998;63-72.
159. Szymusiak et al. Behav. Brain Res. 2000.