The role of cholinergic system in neuronal plasticity: Focus on visual cortex and muscarinic receptors

Archives Italiennes de Biologie

Volumn 146, Issue 3-4, 2008, Pages 165-188

  Origlia, N ^a   Kuczewski, N ^b   Pesavento, E ^b   Aztiria, E ^b   Domenici, Luciano ^a,c  

^a CNR   (Italy)

^b SISSA   (Italy)

^c UNIVERSITY OF L'AQUILA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; ACETYLCHOLINESTERASE; CHOLINE ACETYLTRANSFERASE; CHOLINERGIC RECEPTOR; GLUTAMIC ACID; IONOTROPIC RECEPTOR; MUSCARINIC RECEPTOR; NEUROTRANSMITTER; NICOTINIC RECEPTOR; NORADRENALIN; POTASSIUM CHANNEL KCNQ; VESICULAR ACETYLCHOLINE TRANSPORTER;

ACETYLCHOLINE RELEASE; ALZHEIMER DISEASE; ANATOMICAL VARIATION; ATTENTION; BRAIN CORTEX; BRAIN DEVELOPMENT; BRAIN FUNCTION; CHOLINERGIC SYSTEM; COGNITION; DEGENERATIVE DISEASE; DEPOLARIZATION; DEPTH PERCEPTION; ELECTROPHYSIOLOGY; EXCITATORY POSTSYNAPTIC POTENTIAL; FOREBRAIN; HIPPOCAMPUS; IMMUNOREACTIVITY; LOCOMOTION; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NERVE EXCITABILITY; NONHUMAN; ONTOGENY; PATHOGENESIS; PEDUNCULOPONTINE TEGMENTAL NUCLEUS; REVIEW; SENSORY STIMULATION; SYNAPTIC TRANSMISSION; VISUAL CORTEX; VISUAL STIMULATION; WORKING MEMORY;

ACETYLCHOLINE; ANIMALS; BASAL GANGLIA; HUMANS; NEURONAL PLASTICITY; NEURONS; RECEPTORS, MUSCARINIC; SYNAPTIC TRANSMISSION; VISUAL CORTEX;

EID: 64549141610     PISSN: 00039829     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (184)

1. ABE, K., INOKAWA, M., KASHIWAGI, A. AND YANAGIHARA, T. Amnesia after a discrete basal forebrain lesion. J. Neurol. Neurosurg. Psychiatry, 65: 126-130, 1998.
2. ACQUAS, E., WILSON, C. AND FIBIGER, H.C. Conditioned and unconditioned stimuli increase frontal cortical and hippocampal acetylcholine release: Effects of novelty, habituation, and fear. J. Neurosci., 16: 3089-3096, 1996.
3. ACQUAS, E., WILSON, C. AND FIBIGER, H.C. Pharmacology of sensory stimulation-evoked increases in frontal cortical acetylcholine release. Neuroscience, 85: 73-83, 1998.
4. AIGNER, T.G., WALKER, D.L. AND MISHKIN, M. Comparison of the effects of scopolamine administered before and after acquisition in a test of visual recognition memory in monkeys. Behav. Neural. Biol., 55: 61-67, 1991.
5. AMARAL, D.G. AND INSAUSTI, R. Retrograde transport of D-[3H]-aspartate injected into the monkey amygdaloid complex. Exp. Brain Res., 88: 375-388, 1992.
6. ASHKENAZI, A., PERALTA, E.G., WINSLOW, J.W., RAMACHANDRAN, J. AND CAPON, D.J. Functional diversity of muscarinic receptor subtypes in cellular signal transduction and growth. Trends Pharmacol. Sci., Suppl: 16-22, 1989.
7. AUBERT, I., CECYRE, D., GAUTHIER, S. AND QUIRION, R. Comparative ontogenic profile of cholinergic markers, including nicotinic and muscarinic receptors, in the rat brain. J. Comp. Neurol., 369: 31-55, 1996.
8. AZTIRIA, E., GOTTI, C. AND DOMENICI, L. Alpha7 but not alpha4 AChR subunit expression is regulated by light in developing primary visual cortex. J. Conip. Neurol., 480: 378-391, 2004.
9. BASKERVILLE, K.A., SCHWEITZER, J.B. AND HERRON, P. Effects of cholinergic depletion on experience-dependent plasticity in the cortex of the rat. Neuroscience, 80: 1159-1169, 1997.
10. BEAR, M.F. Bidirectional synaptic plasticity: From theory to reality. Philos. Trans. R. Soc. Lond. B. Biol. Sci., 358: 649-655, 2003.
11. BEAR, M.F. AND SINGER, W. Modulation of visual cortical plasticity by acetylcholine and noradrenaline. Nature, 320: 172-176, 1986.
12. BEAULIEU, C. AND SOMOGYI, P. Enrichment of cholinergic synaptic terminals on GABAergic neurons and coexistence of immunoreactive GABA and choline acetyltransferase in the same synaptic terminals in the striate cortex of the cat. J. Comp. Neurol., 304: 666-680, 1991.
13. BIERER, L.M., HAROUTUNIAN, V., GABRIEL, S., KNOTT, P.J., CARLIN, L.S., PUROHIT, D.P., PERL, D.P., SCHMEIDLER, J., KANOF, P. AND DAVIS, K.L. Neurochemical correlates of dementia severity in Alzheimer's disease: Relative importance of the cholinergic deficits. J. Neurochem., 64: 749-760, 1995.
14. BROCHER, S., ARTOLA, A. AND 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: 27-36, 1992.
15. BROWN, D.A. AND ADAMS, P.R. Muscarinic suppression of a novel voltage-sensitive K+ current in a vertebrate neurone, Nature, 283: 673-676, 1980.
16. BUTCHER, L.L. AND SEMBA, K. Reassessing the cholinergic basal forebrain: Nomenclature schemata and concepts. Trends Neurosci., 12: 483-485, 1989.
17. CALABRESI, P., CENTONZE, D., GUBELLINI, P., PISANI, A. AND BERNARDI, G. Endogenous ACh enhances striatal NMDA-responses via M1-like muscarinic receptors and PKC activation. Eur. J. Neurosci., 10: 2887-2895, 1998.
18. CALARCO, C.A. AND ROBERTSON, R.T. Development of basal forebrain projections to visual cortex: DiI studies in rat. J. Comp. Neurol., 354: 608-626, 1995.
19. CAMPANAC, E. AND DEBANNE, D. Plasticity of neuronal excitability: Hebbian rules beyond the synapse. Archives Italiennes de Biologie, 145: 277-87, 2007.
20. CARR, D.B. AND SURMEIER, D.J. M1 muscarinic receptor modulation of Kir2 channels enhances temporal summation of excitatory synaptic potentials in prefrontal cortex pyramidal neurons. J. Neurophysiol., 97: 3432-3438, 2007.
21. 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: 689-695, 1986.
22. CAULFIELD, M.P. AND BIRDSALL, N.J. International Union of Pharmacology. XVII. Classification of muscarinic acetylcholine receptors. Pharmacol. Rev., 50: 279-290, 1998.
23. CECCARELLI, I., CASAMENTI, F., MASSAFRA, C., PEPEU, G., SCALL C. AND ALOISI, A.M. Effects of novelty and pain on behavior and hippocampal extracellular ACh levels in male and female rats. Brain Res., 815: 169-176, 1999.
24. CELESIA, G.G. AND JASPER, H.H. Acetylcholine released from cerebral cortex in relation to state of activation. Neurology, 16: 1053-1063, 1966.
25. CHAMPTIAUX, N. AND CHANGEUX, J.P. Knock-out and knock-in mice to investigate the role of nicotinic receptors in the central nervous system. Curr. Drug Targets CNS Neurol. Disord., 1: 319-330, 2002.
26. CHARNET, P., LABARCA, C. AND LESTER, H.A. Structure of the gamma-less nicotinic acetylcholine receptor: Learning from omission. Mol. Pharmacol., 41: 708-717, 1992.
27. CHEONG, M.Y., YUN, S.H., MOOK-JUNG, I., JOO, I., HUH, K. AND JUNG, M.W. Cholinergic modulation of synaptic physiology in deep layer entorhinal cortex of the rat. J. Neurosci. Res., 66: 117-121, 2001.
28. CHOI, S.Y., CHANG, J., JIANG, B., SEOL, G.H., MIN, S.S., HAN, J.S., SHIN, H.S., GALLAGHER, M. AND KIRKWOOD, A. Multiple receptors coupled to phospholipase C gate long-term depression in visual cortex. J. Neurosci., 25: 11433-11443, 2005.
29. CONNER, J.M., CULBERSON, A., PACKOWSKI, C., CHIBA, A.A. AND TUSZYNSKI, M.H. Lesions of the Basal forebrain cholinergic system impair task acquisition and abolish cortical plasticity associated with motor skill learning. Neuron, 38: 819-829, 2003.
30. COX, C.L., METHERATE, R. AND ASHE, J.H. Modulation of cellular excitability in neocortex: Muscarinic receptor and second messenger-mediated actions of acetylcholine. Synapse, 16: 123-136, 1994.
31. COX, T. AND TYE, N. Effects of physotigmine on the acquisition of a position discrimination in rats. Neuropharmacology, 12: 477-484, 1973.
32. CULLINAN, W.E. AND ZABORSZKY, L. Organization of ascending hypothalamic projections to the rostral forebrain with special reference to the innervation of cholinergic projection neurons. J. Comp. Neurol., 306: 631-667, 1991.
33. DALLEY, J.W., MCGAUGHY, J., O'CONNELL, M.T., CARDINAL, R.N., LEVITA, L. AND ROBBINS, T.W. Distinct changes in cortical acetylcholine and noradrenaline efflux during contingent and noncontingent performance of a visual attentional task. J. Neurosci., 21: 4908-4914, 2001.
34. DAMASIO, A.R., GRAFF-RADFORD, N.R., ESLINGER, P.J., DAMASIO, H. AND KASSELL, N. Amnesia following basal forebrain lesions. Arch. Neurol., 42: 263-271, 1985.
35. DESCARRIES L. The hypothesis of an ambient level of acetylcholine in the central nervous system. J. Physiol. Paris, 92 (3-4): 215-20, Jun-Aug 1998.
36. DESCARRIES, L., BEAUDET, A. AND WATKINS, K.C. Serotonin nerve terminals in adult rat neocortex. Brain Res., 100: 563-588, 1975.
37. DESCARRIES, L., GISIGER, V. AND STERIADE M. Diffuse transmission by acetylcholine in the CNS. Prog. Neurobiol., 53: 603-625, 1997.
38. DEUTSCH, J.A. The cholinergic synapse and the site of memory. Science, 174: 788-794, 197 1.
39. DI ANGELANTONIO, S., MATTEONI, C., FABBRETTI, E. AND NISTRI A. Molecular biology and electrophysiology of neuronal nicotinic receptors of rat chromaffin cells. Eur. J. Neurosci., 17: 2313-2322, 2003.
40. DIAMOND, B.J., DE LUCA, J. AND KELLEY, S.M. Memory and executive functions in amnesic and non-amnesic patients with aneurysms of the anterior communicating artery. Brain, 120 (Pt 6): 1015-1025, 1997.
41. DINOPOULOS, A., EADIE, L.A., DORI, I. AND PARNAVELAS, J.G. The development of basal forebrain projections to the rat visual cortex. Exp. Brain Res., 76: 563-571, 1989.
42. DISNEY, A.A., DOMAKONDA, K.V. AND AOKI, C. Differential expression of muscarinic acetylcholine receptors across excitatory and inhibitory cells in visual cortical areas V1 and V2 of the macaque monkey. J. Comp. Neurol., 499: 49-63, 2006.
43. DONOGHUE, J.P. AND CARROLL, K.L. Cholinergic modulation of sensory responses in rat primary somatic sensory cortex. Brain Res., 408: 367-371, 1987.
44. ECKENSTEIN, F. AND BAUGHMAN, R.W. Two types of cholinergic innervation in cortex, one co-localized with vasoactive intestinal polypeptide. Nature, 309: 153-155, 1984.
45. ECKENSTEIN, F.P., BAUGHMAN, R.W. AND QUINN, J. An anatomical study of cholinergic innervation in rat cerebral cortex. Neuroscience, 25: 457-474, 1988.
46. ERISIR, A., LEVEY, A.I. AND AOKI, C. Muscarinic receptor M(2) in cat visual cortex: Laminar distribution, relationship to gamma-aminobutyric acidergic neurons, and effect of cingulate lesions. J. Comp. Neurol., 441: 168-185, 2001.
47. EVERITT, B.J. AND ROBBINS, T.W. Central cholinergic systems and cognition. Annu, Rev. Psychol., 48: 649-684, 1997.
48. FADDA, F., COCCO, S. AND STANCAMPIANO, R. Hippocampal acetylcholine release correlates with spatial learning performance in freely moving rats. Neuroreport, 11: 2265-2269, 2000.
49. FELLER, M.B. The role of nAChR-mediated spontaneous retinal activity in visual system development. J. Neurobiol., 53: 556-567, 2002.
50. FISCHER, W., NILSSON, O.G. AND 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., 556: 44-52, 1991.
51. FOSSE, V.M., HEGGELUND, P. AND FONNUM, F. Postnatal development of glutamatergic, GABAergic, and cholinergic neurotransmitter phenotypes in the visual cortex, lateral geniculate nucleus, pulvinar, and superior colliculus in cats. J Neurosci., 9: 426-435, 1989.
52. FRASER, D.D. AND MACVICAR, B.A. Cholinergic-dependent plateau potential in hippocampal CA1 pyramidal neurons. J Neurosci., 16: 4113-4128, 1996.
53. FREO, U., RICCIARDI E., PIETRINI P., SCHAPIRO, M.B., RAPOPORT, S.I. AND FUREY, M.L. Pharmacological modulation of prefrontal cortical activity during a working memory task in young and older humans: A PET study with physostigmine. Am. J. Psychiatry, 162: 2061-70, 2005.
54. FREUND, T.F. GABAergic septohippocampal neurons contain parvalbumin. Brain Res., 478: 375-381, 1999.
55. FREUND, T.F. AND GULYAS, A.I. GABAergic interneurons containing calbindin D28K or somatostatin are major targets of GABAergic basal forebrain afferents in the rat neocortex. J. Comp. Neurol., 314: 187-199, 1991.
56. FUCILE, S. Ca2+ permeability of nicotinic acetylcholine receptors. Cell Calcium, 35: 1-8, 2004.
57. FURMANSKI, C.S., SCHLUPPECK, D. AND ENGEL, S.A. Learning strengthens the response of primary visual cortex to simple patterns. Curr. Biol., 14: 573-578, 2004.
58. FUREY, M.L., PIETRINI, P. AND HAXBY, J.V. Cholinergic enhancement and increased selectivity of perceptual processing during working memory. Science, 290: 2315-2319, 2000.
59. FUREY, M.L., PIETRINI, P., ALEXANDER, G.E., SCHAPIRO, M.B. AND HORWITZ, B. Cholinergic enhancement improves performance on working memory by modulating the functional activity in distinct brain regions: a positron emission tomography regional cerebral blood flow study in healthy humans. Brain Res. Bull., 51: 213-218, 2000.
60. FUREY, M.L., RICCIARDI, E., SCHAPIRO, M.B., RAPOPORT, S.I. AND PIETRINI, P. Cholinergic enhancement eliminates modulation of neural activity by task difficulty in the prefrontal cortex during working memory. J. Cogn. Neurosci., 20: 1342-1353, 2008.
61. FUXE, K., DAHLSTROM, A., HOISTAD, M., MARCELLINO, D., JANSSON, A., RIVERA, A., DIAZ-CABIALE, Z., JACOBSEN, K., TINNER-STAINES, B., HAGMAN, B., LEO, G., STAINES, W., GUIDOLIN, D., KEHR, J., GENEDANI, S., BELLUARDO, N. AND AGNATI, L.F. From the Golgi-Cajal mapping to the transmitter-based characterization of the neuronal networks leading to two modes of brain communication: Wiring and volume transmission. Brain Res. Rev., 55: 17-54, 2007.
62. GIL, Z., CONNORS, B.W. AND AMITAI, Y. Differential regulation of neocortical synapses by neuromodulators and activity. Neuron, 19: 679-686, 1997.
63. GIOVANNINI, M.G., RAKOVSKA, A., BENTON, R.S, PAZZAGLI, M., BIANCHI, L. AND PEPEU, G. Effects of novelty and habituation on acetylcholine, GABA, and glutamate release from the frontal cortex and hippocampus of freely moving rats. Neuroscience, 106: 43-53, 2001.
64. GOLMAYO, L., NUNEZ, A. AND ZABORSZKY, L. Electrophysiological evidence for the existence of a posterior cortical-prefrontal-basal forebrain circuitry in modulating sensory responses in visual and somatosensory rat cortical areas. Neuroscience, 119: 597-609, 2003.
65. GOTTI, C. AND CLEMENTI, F. Neuronal nicotinic receptors: From structure to pathology. Prog. Neurobiol., 74: 363-396, 2004.
66. GOULD, E., WOOLF, N.J. AND BUTCHER, L.L. Postnatal development of cholinergic neurons in the rat: I. Forebrain. Brain Res. Bull., 27: 767-789, 1991.
67. GRUBB, M.S., ROSSI, F.M., CHANGEUX, J.P. AND THOMPSON, I.D. Abnormal functional organization in the dorsal lateral geniculate nucleus of mice lacking the beta 2 subunit of the nicotinic acetylcholine receptor. Neuron, 40: 1161-1172, 2003.
68. GU, Q. AND SINGER, W. Effects of intracortical infusion of anticholinergic drugs on neuronal plasticity in kitten striate cortex. Eur. J. Neurosci., 5: 475-485, 1993.
69. HAJ-DAHMANE, S. AND ANDRADE, R. Ionic mechanism of the slow afterdepolarization induced by muscarinic receptor activation in rat prefrontal cortex. J Neurophysiol, 80: 1197-1210, 1998.
70. HAJ-DAHMANE, S. AND ANDRADE, R. Muscarinic receptors regulate two different calcium-dependent non-selective cation currents in rat prefrontal cortex. Eur. J. Neurosci., 11: 1973-1980, 1999.
71. HAMAM, B.N., SINAI, M., POIRIER, G. AND CHAPMAN, C.A. Cholinergic suppression of excitatory synaptic responses in layer II of the medial entorhinal cortex. Hippocampus, 17: 103-113, 2007.
72. HANES, M.A., ROBERTSON, R.T. AND YU, J. Transition from developing to mature patterns of acetylcholinesterase activity in rat visual cortex: Implications for the time-course of geniculocortical development. Brain Res. Dev. Brain Res., 66: 97-108, 1992.
73. HASSELMO, M.E. AND BOWER, J.M. Cholinergic suppression specific to intrinsic not afferent fiber synapses in rat piriform (olfactory) cortex. J. Neurophysiol., 67: 1222-1229, 1992.
74. HASSELMO, M.E. AND CEKIC, M. Suppression of synaptic transmission may allow combination of associative feedback and self-organizing feedforward connections in the neocortex. Behav. Brain Res., 79: 153-161, 1996.
75. HENDERSON, Z. The projection from the striaturn to the nucleus basalis in the rat: An electron microscopic study. Neuroscience, 78: 943-955, 1997.
76. HIRONAKA, N., TANAKA, K., IZAKI, Y., HORI, K. AND NOMURA, M. Memory-related acetylcholine efflux from rat prefrontal cortex and hippocampus: A microdialysis study. Brain Res., 901: 143-150, 2001.
77. HOHMANN, C.F., POTTER, E.D. AND LEVEY A.I. Development of muscarinic receptor subtypes in the forebrain of the mouse. J. Comp. Neurol., 358: 88-101, 1995.
78. HOUSER, C.R., CRAWFORD, G.D., BARBER, R.P., SALVATERRA, P.M. AND VAUGHN, J.E. Organization and morphological characteristics of cholinergic neurons: An immunocytochemical study with a monoclonal antibody to choline acetyltransferase. Brain Res., 266: 97-119, 1983.
79. HOUSER, C.R., CRAWFORD, G.D., SALVATERRA, P.M. AND VAUGHN, J.E. Immunocytochemical localization of choline acetyltransferase in rat cerebral cortex: A study of cholinergic neurons and synapses. J Comp Neurol, 234: 17-34, 1985.
80. HUBEL, D.H. AND WIESEL, T.N. Brain mechanisms of vision. Sci. Am., 241: 150-162, 1979.
81. HUBEL, D.H. AND WIESEL, T.N. Early exploration of the visual cortex. Neuron, 20: 401-412, 1998.
82. ICHIKAWA, T., AJIKI, K., MATSUURA, J. AND MISAWA, H. Localization of two cholinergic markers, choline acetyltransferase and vesicular acetylcholine transporter in the central nervous system of the rat: In situ hybridization histochemistry and immunohistochemistry. J. Chem. Neuroanat., 13: 23-39, 1997.
83. JASPER, H.H. AND TESSIER, J. Acetylcholine liberation from cerebral cortex during paradoxical (REM) sleep. Science, 172: 601-602, 1971.
84. JOLKKONEN, E., MIETTINEN, R., PIKKARAINEN, M. AND PITKANEN, A. Projections from the amygdaloid complex to the magnocellular cholinergic basal forebrain in rat. Neuroscience, 111: 133-149, 2002.
85. JULIANO, S.L., MA, W. AND ESLIN, D. Cholinergic depletion prevents expansion of topographic maps in somatosensory cortex. Proc. Natl. Acad Sci. USA, 88: 780-784, 1991.
86. KAMETANI, H. AND KAWAMURA, H. Alterations in acetylcholine release in the rat hippocampus during sleep-wakefulness detected by intracerebral dialysis. Life Sci., 47: 421-426, 1990.
87. KARNI, A. AND SAGI, D. Where practice makes perfect in texture discrimination: Evidence for primary visual cortex plasticity. Proc. Natl. Acad. Sci. USA, 88: 4966-4970, 1991.
88. KILGARD, M.P. AND MERZENICH, M.M. Cortical map reorganization enabled by nucleus basalis activity. Science, 279: 1714-1718, 1998.
89. KIMURA, F. Cholinergic modulation of cortical function: A hypothetical role in shifting the dynamics in cortical network. Neurosci. Res., 38: 19-26, 2000.
90. KIMURA, F. AND BAUGHMAN, R.W. Distinct muscarinic receptor subtypes suppress excitatory and inhibitory synaptic responses in cortical neurons. J. Neurophysiol., 77: 709-716, 1997.
91. KIRKWOOD, A., LEE, H.-K. AND BEAR, M.F. Co-regulation of long-term potentiation and experience-dependent synaptic plasticity in visual cortex by age and experience. Nature, 375: 328-331, 1995.
92. KIRKWOOD, A., ROZAS, C., KIRKWOOD, J., PEREZ, F. AND BEAR, M.F. Modulation of long-term synaptic depression in visual cortex by acetylcholine and norepinephrine. J. Neurosci., 19: 1599-1609, 1999.
93. KLINK, R. AND ALONSO, A. Muscarinic modulation of the oscillatory and repetitive firing properties of entorhinal cortex layer II neurons. J. Neurophysiol., 77: 1813-1828, 1997.
94. KRETTEK, J.E. AND PRICE, J.L. Amygdaloid projections to subcortical structures within the basal forebrain and brainstem in the rat and cat. J. Comp. Neurol., 178: 225-254, 1978.
95. KRNJEVIC, K. AND PHILLIS, J.W. Acetylcholine-sensitive cells in the cerebral cortex. J. Physiol., 166. 296-327, 1963.
96. KRNJEVIC, K., PUMAIN, R. AND RENAUD, L. The mechanism of excitation by acetylcholine in the cerebral cortex. J. Physiol., 215: 247-268, 1971.
97. KUCZEWSKI, N., AZTIRIA, E., GAUTAM, D., WESS, J. AND DOMENICI, L. Acetylcholine modulates cortical synaptic transmission via different muscarinic receptors, as studied with receptor knockout mice. J. Physiol., 566: 907-919, 2005a.
98. KUCZEWSKI, N., AZTIRIA, E., LEANZA, G. AND DOMENICI, L. Selective cholinergic immunolesioning affects synaptic plasticity in developing visual cortex. Eur. J. Neurosci., 21: 1807-1814, 2005b.
99. KUROSAWA, M., SATO, A. AND SATO, Y. Stimulation of the nucleus basalis of Meynert increases acetylcholine release in the cerebral cortex in rats. Neurosci. Lett., 98: 45-50, 1989.
100. LAMBE, E.K., PICCIOTTO, MR. AND AGHAJANIAN, G.K. Nicotine induces glutamate release from thalamocortical terminals in prefrontal cortex. Neuropsychopharmacology, 28: 216-225, 2003.
101. LAPLANTE, F., MORIN, Y., QUIRION, R. AND 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, 132: 501-510, 2005.
102. LAVOIE, B. AND PARENT, A. Pedunculopontine nucleus in the squirrel monkey: Cholinergic and glutamatergic projections to the substantia nigra. J. Comp. Neurol., 344: 232-241, 1994.
103. LAZARENO, S. AND BIRDSALL, N.J. Detection, quantitation, and verification of allosteric interactions of agents with labeled and unlabeled ligands at G protein-coupled receptors: Interactions of strychnine and acetylcholine at muscarinic receptors. Mol. Pharmacol., 48: 362-378, 1995.
104. LEANZA, G., NILSSON, O.G., WILEY, R.G. AND BJORKLUND, A. Selective lesioning of the basal forebrain cholinergic system by intraventricular 192 IgG-saporin: Behavioural, biochemical and stereological studies in the rat. Eur. J. Neurosci., 7: 329-343, 1995.
105. LEVEY, A.I. Muscarinic acetylcholine receptor expression in memory circuits: Implications for treatment of Alzheimer disease. Proc. Natl. Acad. Sci. USA, 93: 13541-13546, 1996.
106. LEVEY, A.I., KITT, C.A., SIMONDS, W.F., PRICE, D.L. AND BRANN, M.R. Identification and localization of muscarinic acetylcholine receptor proteins in brain with subtype-specific antibodies. J. Neurosci., 11: 3218-3226, 1991.
107. LEVEY, A.I., WAINER, B.H., RYE, D.B., MUFSON, E.J. AND MESULAM, M.M. Choline acetyltransferase-immunoreactive neurons intrinsic to rodent cortex and distinction from acetylcholinesterase-positive neurons. Neuroscience, 13: 341-353, 1984.
108. LEVY, R.B. AND AOKI, C. Alpha7 nicotinic acetylcholine receptors occur at postsynaptic densities of AMPA receptor-positive and -negative excitatory synapses in rat sensory cortex. J. Neurosci., 22: 5001-5015, 2002.
109. MARINI, G., CALVANI, M., CECCARELLI, P. AND MANCIA, M. Behavioral and electrophysiological changes induced by acetyl-L-carnitine in aged freely-moving rats. Archives Italiennes de Biologie, 144: 33-43, 2006.
110. MARTINEZ-GUIJARRO, F.J. AND FREUND, T.F. Distribution of GABAergic interneurons immunoreactive for calretinin, calbindin D28K, and parvalbumin in the cerebral cortex of the lizard Podarcis hispanica. J. Comp. Neurol., 322: 449-460, 1992.
111. MCCORMICK, D.A. Actions of acetylcholine in the cerebral cortex and thalamus and implications for function. Prog. Brain Res., 98: 303-308, 1993.
112. MCCORMICK, D.A. AND PRINCE, D.A. Actions of acetylcholine in the guinea-pig and cat medial and lateral geniculate nuclei, in vitro. J. Physiol., 392: 147-165, 1987.
113. MCCORMICK, D.A. AND PRINCE, D.A. Mechanisms of action of acetylcholine in the guinea-pig cerebral cortex in vitro. J. Physiol., 375: 169-194, 1986.
114. MCCORMICK, D.A. AND PRINCE, D.A. Two types of muscarinic response to acetylcholine in mammalian cortical neurons, Proc. Natl. Acad Sci. USA, 82: 6344-6348, 1985.
115. MCDONALD, J.K., SPECIALE, S.G. AND PARNAVELAS, J.G. The laminar distribution of glutamate decarboxylase and choline acetyltransferase in the adult and developing visual cortex of the rat. Neuroscience, 21: 925-932, 1997.
116. 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: 247-265, 1996.
117. MECHAWAR, N., COZZARI, C. AND DESCARRIES, L. Cholinergic innervation in adult rat cerebral cortex: A quantitative immunocytochemical description. J. Comp. Neurol., 428: 305-318, 2000.
118. MECHAWAR, N., WATKINS, K.C. AND DESCARRIES, L. Ultrastructural features of the acetylcholine innervation in the developing parietal cortex of rat. J. Comp. Neurol., 443: 250-258, 2002.
119. MELZER, P., MINEO, L. AND EBNER, F.F. Optic nerve transection affects development and use-dependent plasticity in neocortex of the rat: Quantitative acetylcholinesterase imaging. Brain Res., 1139: 68-84, 2007.
120. 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 (Ch1-Ch6). Neuroscience, 10: 1185-1201, 1983.
121. METHERATE, R. AND HSIEH, C.Y. Regulation of glutamate synapses by nicotinic acetylcholine receptors in auditory cortex. Neurobiol. Learn. Mem., 80: 285-290, 2003.
122. MIZOGUCHI, K., YUZURIHARA, M., ISHIGE, A., SASAKI, H. AND TABIRA, T. Effect of chronic stress oin cholinergic transmission in rat hippocampus. Brain Res., 915: 108-111, 2001.
123. MRZLJAK, L., LEVEY, A.I. AND GOLDMAN-RAKIC, P.S. Association of m1 and m2 muscarinic receptor proteins with asymmetric synapses in the primate cerebral cortex: Morphological evidence for cholinergic modulation of excitatory neurotransmission. Proc. Natl. Acad. Sci. USA, 90: 5194-5198, 1993.
124. MRZLJAK, L., PAPPY, M., LERANTH, C. AND GOLDMAN-RAKIC, P.S. Cholinergic synaptic circuitry in the macaque prefrontal cortex. J. Comp. Neurol., 357: 603-617, 1995.
125. NAIL-BOUCHERIE, K., DOURMAP, N., JAFFARD, R. AND COSTENTIN, J. Contextual fear conditioning is associated with an increase of acetylcholine release in the hippocampus of rat. Cogn. Brain. Res., 9: 193-197, 2000.
126. OLDFORD, E. AND CASTRO-ALAMANCOS, M.A. Input-specific effects of acetylcholine on sensory and intracortical evoked responses in the "barrel cortex" in vivo. Neuroscience, 117: 769-778, 2003.
127. ORIGLIA, N., CAPSONI, S., DOMENICI, L. AND CATTANEO, A. Time window in cholinomimetic ability to rescue long-term potentiation in neurodegenerating anti-nerve growth factor mice. J. Alzheimers Dis., 9: 59-68, 2006.
128. ORIGLIA, N., KUCZEWSKI, N., AZTIRIA, E., GAUTAM. D., WESS, J. AND DOMENICI, L. Muscarinic acetylcholine receptor knockout mice show distinct synaptic plasticity impairments in the visual cortex. J. Physiol., 577: 829-840, 2006.
129. ORSETTI, M., CASAMENTI, F. AND PEPEU, G. Enhanced acetylcholine release in the hippocampus and cortex during acquisition of an operant behavior. Brain Res, 724: 89-96, 1996.
130. PAGE, K.M., CURTIS, C.A., JONES, P.G. AND HULME, E.C. The functional role of the binding site aspartate in muscarinic acetylcholine receptors, probed by site-directed mutagenesis. Eur. J. Pharmacol., 289: 429-437, 1995.
131. PAPKE, R.L. AND HEINEMANN, S.F. The role of the beta 4-subunit in determining the kinetic properties of rat neuronal nicotinic acetylcholine alpha 3-receptors. J. Physiol., 440: 95-1129 1991.
132. PARKINSON, D., KRATZ, K.E. AND DAW, N.W. Evidence for a nicotinic component to the actions of acetylcholine in cat visual cortex. Exp. Brain Res., 73: 553-568, 1988.
133. PASSETTI, F., DALLEY, JW., O'CONNELL, M.T., EVERITT, B.J. AND ROBBINS, T.W. Increased acetylcholine release in the rat medial prefrontal cortex during performance of a visual attentional task. Eur. J. Neurosci., 12: 3051-3058, 2000.
134. PAUS, T., JECH, R., THOMPSON, C.J., COMEAU, R., PETERS, T. AND EVANS, A.C. Transcranial magnetic stimulation during positron emission tomography: A new method for studying connectivity of the human cerebral cortex. J. Neurosci., 17: 3178-3184, 1997.
135. PEDATA, F., SLAVIKOVA, J., KOTAS, A. AND PEPEU, G. Acetylcholine release from rat cortical slices during postnatal development and aging. Neurobiol. Aging, 4: 31-35, 1983.
136. PENSCHUCK, S., CHEN-BEE, C.H., PRAKASH, N. AND FROSTIG, R.D. In vivo modulation of a cortical functional sensory representation shortly after topical cholinergic agent application. J. Comp. Neurol., 452: 38-50, 2002.
137. PEPEU, G. AND GIOVANNINI M.G. Changes in acetylcholine extracellular levels during cognitive processes. Learn. Mem., 11: 21-27, 2004.
138. PERRY, E.K., TOMLINSON, B.E., BLESSED, G., BERGMANN, K., GIBSON, P.H. AND PERRY, R.H. Correlation of cholinergic abnormalities with senile plaques and mental test scores in senile dementia. Br. Med. J., 2: 1457-1459, 1978.
139. PESAVENTO, E., CAPSONI, S., DOMENICI, L. AND CATTANEO, A. Acute cholinergic rescue of synaptic plasticity in the neurodegenerating cortex of anti-nerve-growth-factor mice. Eur. J. Neurosci., 15: 1030-1036, 2002.
140. PESAVENTO, E., MARGOTTI, E., RIGHI, M., CATTANEO, A. AND DOMENICI, L. Blocking the NGF-TrkA interaction rescues the developmental loss of LTP in the rat visual cortex: Role of the cholinergic system. Neuron, 25: 165-175, 2000.
141. POLAT, U., MA-NAIM, T., BELKIN, M. AND SAGI, D. Improving vision in adult amblyopia by perceptual learning. Proc. Natl. Acad. Sci. USA, 101: 6692-6697, 2004.
142. RAO, Y. AND DAW, N.W. Layer variations of long-term depression in rat visual cortex. J. Neurophysiol., 92: 2652-2658, 2004.
143. RASMUSSON, D.D., SZERB, I.C. AND 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, 72: 419-427, 1996.
144. ROSSI, F.M., PIZZORUSSO, T., PORCIATTI, V., MARUBIO, L.M., MAFFEI, L. AND CHANGEUX, J.P. Requirement of the nicotinic acetylcholine receptor beta 2 subunit for the anatomical and functional development of the visual system, Proc. Natl. Acad. Sci. USA, 98: 6453-6458, 2001.
145. RYE, D.B., WAINER, B.H., MESULAM, M.M., MUFSON, E.J. AND SAPER, C.B. Cortical projections arising from the basal forebrain: A study of cholinergic and noncholinergic components employing combined retrograde tracing and immunohistochemical localization of choline acetyltransferase. Neuroscience, 13: 627-643, 1984.
146. SARTER, M. AND BRUNO, J.P. Cortical cholinergic inputs mediating arousal, attentional processing and dreaming: Differential afferent regulation of the basal forebrain by telencephalic and brainstem afferents. Neuroscience, 95: 933-952, 2000.
147. SATO, H., HATA, Y., MASUI, H. AND TSUMOTO, T. A functional role of cholinergic innervation to neurons in the cat visual cortex. J. Neurophysiol., 58: 765-780, 1987.
148. SATO, H., KATSUYAMA, N., TAMURA, H., HATA, Y. AND TSUMOTO, T. Mechanisms underlying orientation selectivity of neurons in the primary visual cortex of the macaque. J. Physiol., 494: (Pt 3): 757-771, 1996.
149. SAWTELL, N.B., FRENKEL, M.Y., PHILPOT, B.D., NAKAZAWA, K., TONEGAWA, S. AND BEAR, M.F. NMDA receptor-dependent ocular dominance plasticity in adult visual cortex. Neuron, 38: 977-985, 2003.
150. SCHLIEBS, R., ROSSNER, S., KUMAR, A. AND BIGL, V. Muscarinic acetylcholine receptor subtypes in rat visual cortex - a comparative study using quantitative receptor autoradiography and in situ hybridization. Indian J. Exp. Biol., 32: 25-30, 1994.
151. SEFTON, A.J. AND DREHER, B. The Rat Nervous System, Ed. Paxinos G. 1995, New York: Academic., 1003-1015.
152. SEMBA, K. AND FIBIGER, H.C. Time of origin of cholinergic neurons in the rat basal forebrain. J. Comp. Neurol., 269: 87-95, 1988a.
153. SEMBA, K., REINER, P.B., McGEER, E.G. AND FIBIGER, H.C. Brainstem afferents to the magnocellular basal forebrain studied by axonal transport, immunohistochemistry, and electrophysiology in the rat. J. Comp. Neurol., 267: 433-453, 1988b.
154. SICILIANO, R., FONTANESI, G., CASAMENTI, F., BERARDI, N., BAGNOLI, P. AND DOMENICI, L. Postnatal development of functional properties of visual cortical cells in rats with excitotoxic lesions of basal forebrain cholinergic neurons. Vis. Neurosci., 14: 111-123, 1997.
155. SILLITO, A.M. AND KEMP, J.A. Cholinergic modulation of the functional organization of the cat visual cortex. Brain Res., 289: 143-155, 1983.
156. SPENCER, D.G. JR., PONTECORVO, M.J. AND HEISE, G.A. Central cholinergic involvement in working memory: Effects of scopolamine on continuous nonmatching and discrimination performance in the rat. Behav. Neurosci., 99: 1049-1065, 1985.
157. STERIADE, M. The intact and sliced brain. 2001, Cambridge: MIT Press., 1-336.
158. STERIADE, M., DOSSI, R.C., PARE, D. AND OAKSON, G. Fast oscillations (20-40 Hz) in thalamocortical systems and their potentiation by mesopontine cholinergic nuclei in the cat. Proc. Natl. Acad. Sci. USA, 88: 4396-4400, 1991.
159. STONE, T.W. Cholinergic mechanisms in the rat somatosensory cerebral cortex. J. Physiol., 225: 485-499, 1972.
160. THIEL, C.M., HUSTON, J.P. AND SCHWARTING, R.K. Cholinergic activation in frontal cortex and nucleus accumbens related to basic behavioral manipulations: Handling, and the role of post-handling experience. Brain Res., 812: 121-132, 1998.
161. TIGGES, M., TIGGES, J., REES, H., RYE, D. AND LEVEY, A.I. Distribution of muscarinic cholinergic receptor proteins m1 to m4 in area 17 of normal and monocularly deprived rhesus monkeys. J. Comp. Neurol., 388: 130-145, 1997.
162. TSANOV, M. AND MANAHAN-VAUGHAN, D. The adult visual cortex expresses dynamic synaptic plasticity that is driven by the light/dark cycle. J. Neurosci., 27: 8414-8421, 2007.
163. UMBRIACO, D., GARCIA, S., BEAULIEU, C. AND DESCARRIES, L. Relational features of acetylcholine, noradrenaline, serotonin and GABA axon terminals in the stratum radiatum of adult rat hippocampus (CA1). Hippocampus, 5: 605-20, 1995.
164. UMBRIACO, D., WATKINS, K.C., DESCARRIES, L., COZZARI, C. AND HARTMAN, B.K. Ultrastructural and morphometric features of the acetylcholine innervation in adult rat parietal cortex: An electron microscopic study in serial sections. J. Comp. Neurol., 348: 351-373, 1994.
165. VAN DER ZEE, E.A. AND LUITEN, P.G. Muscarinic acetylcholine receptors in the hippocampus, neocortex and amygdala: A review of immunocytochemical localization in relation to learning and memory. Prog. Neurobiol., 58: 409-471, 1999.
166. VIDAL, C. AND CHANGEUX, J.P. Nicotinic and muscarinic modulations of excitatory synaptic transmission in the rat prefrontal cortex in vitro. Neuroscience, 56: 23-32, 1993.
167. WADA, E., WADA, K., BOULTER, J., DENERIS, E., HEINEMANN, S., PATRICK, J. AND SWANSON, L.W. Distribution of alpha 2, alpha 3, alpha 4, and beta 2 neuronal nicotinic receptor subunit mRNAs in the central nervous system: A hybridization histochemical study in the rat. J. Comp. Neurol., 284: 314-335, 1989.
168. WAINER, B.H. AND RYE, D.B. Retrograde horseradish peroxidase tracing combined with localization of choline acetyltransferase immunoreactivity. J. Histochem. Cytochem., 32: 439-443, 1984.
169. WAITE, J.J. AND THAL, L.J. Lesions of the cholinergic nuclei in the rat basal forebrain: Excitotoxins vs. an immunotoxin. Life Sci., 58: 1947-1953, 1996.
170. WANG, L.Y., GAN, L., FORSYTHE, I.D. AND KACZMAREK, L.K. Contribution of the Kv3.1 potassium channel to high-frequency firing in mouse auditory neurones. J. Physiol., 509 (Pt 1): 183-194, 1998.
171. WANG, Z. AND MCCORMICK, D.A. Control of firing mode of corticotectal and corticopontine layer V burst-generating neurons by norepinephrine, acetylcholine, and IS,3R-ACPD. J. Neurosci., 13: 2199-2216, 1993.
172. WEI, J., WALTON, E.A., MILICI, A. AND BUCCAFUSCO, J.J. m1-m5 muscarinic receptor distribution in rat CNS by RT-PCR and HPLC. J. Neurochem., 63: 815-821, 1994.
173. WESS, J. Molecular biology of muscarinic acetylcholine receptors. Crit. Rev. Neurobiol., 10: 69-99, 1996.
174. WESS, J. Novel insights into muscarinic acetylcholine receptor function using gene targeting technology. Trends Pharmacol. Sci., 24: 414-420, 2003.
175. WHITING, P. AND LINDSTROM, J. Pharmacological properties of immuno-isolated neuronal nicotinic receptors. J. Neurosci., 6: 3061-3069, 1986.
176. WHITING, P.J., COOPER, I. AND LINDSTROM, J.M. Antibodies in sera from patients with myasthenia gravis do not bind to nicotinic acetylcholine receptors from human brain. J. Neuroimmunol., 16: 205-213, 1987.
177. WONNACOTT, S. Presynaptic nicotinic ACh receptors. Trends Neurosci., 20: 92-98, 1997.
178. XIANG, Z., HUGUENARD, J.R. AND PRINCE, D.A. Cholinergic switching within neocortical inhibitory networks. Science, 281: 985-988, 1998.
179. YUN, S.H., CHEONG, M.Y., MOOK-JUNG, I., HUH, K., LEE, C. AND JUNG, M.W. Cholinergic, modulation of synaptic transmission and plasticity in entorhinat cortex and hippocampus of the rat. Neuroscience, 97: 671-676, 2000.
180. ZHANG, W., BASILE, A.S., GOMEZA, J., VOLPICELLI, L.A., LEVEY, A.I. AND WESS, J. Characterization of central inhibitory muscarinic autoreceptors by the use of muscarinic acetylcholine receptor knock-out mice. J. Neurosci., 22: 1709-1717, 2002.
181. ZHU, X.O., DE PERMENTIER, P.J. AND WAITE, P.M. Cholinergic depletion by IgG192-saporin retards development of rat barrel cortex. Brain Res. Dev. Brain Res., 136: 1-16, 2002.
182. ZHU, X.O. AND WAITE, P.M. Cholinergic depletion reduces plasticity of barrel field cortex. Cereb. Cortex, 8: 63-72, 1998.
183. ZINKE, W., ROBERTS, M.J., GUO, K., MCDONALD, J.S., ROBERTSON, R. AND THIELE, A. Cholinergic modulation of response properties and orientation tuning of neurons in primary visual cortex of anaesthetized Marmoset monkeys. Eur. J. Neurosci., 24: 314-328, 2006.
184. ZMAROWSKI, A., SARTER, M. AND BRUNO, J.P. Glutamate receptors in nucleus accumbens mediate regionally selective increases in cortical acetylcholine release. Synapse, 61: 115-123, 2007.