Cholinergic systems mediate action from movement to higher consciousness

Behavioural Brain Research

Volumn 221, Issue 2, 2011, Pages 488-498

  Woolf, Nancy J ^a   Butcher, Larry L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cortex; Intracellular skeleton; Motor actions; Muscarinic; Muscle; Nicotinic

Indexed keywords

ACTIN; MICROTUBULE PROTEIN; MUSCARINIC RECEPTOR; NEUROTRANSMITTER; NICOTINIC RECEPTOR;

ACETYLCHOLINE RELEASE; AMYGDALOID NUCLEUS; AROUSAL; ASSOCIATION CORTEX; ATTENTION; AUDITORY CORTEX; BRAIN FUNCTION; BRAIN MAPPING; CHOLINERGIC SYSTEM; COGNITION; CONSCIOUSNESS; CORPUS STRIATUM; CYTOSKELETON; DENDRITE; EPITHALAMUS; LEARNING; MEMORY; MEYNERT BASAL NUCLEUS; MUSCLE CONTRACTION; NERVE CELL PLASTICITY; NEUROMODULATION; NEUROMUSCULAR SYNAPSE; NEUROTRANSMISSION; NONHUMAN; PERCEPTION; PONTINE NUCLEUS; PRIORITY JOURNAL; REVIEW; SARCOPLASMIC RETICULUM; SKELETAL MUSCLE; SYNAPTOGENESIS; VISUAL CORTEX;

ANIMALS; BRAIN; CHOLINERGIC FIBERS; COGNITION; CYTOSKELETON; HUMANS; MODELS, NEUROLOGICAL; MOVEMENT; MUSCLE CONTRACTION; NERVE NET; SYNAPTIC TRANSMISSION;

EID: 79955713813     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2009.12.046     Document Type: Review

References (188)

1. Abu-Shakra S.R., Cole A.J., Adams R.N., Drachman D.B. Cholinergic stimulation of skeletal muscle cells induces rapid immediate early gene expression: role of intracellular calcium. Mol Brain Res 1994, 26:55-60.
2. Acquas E., Wilson C., Fibiger H.C. Conditioned and unconditioned stimuli increase frontal cortical and hippocampal acetylcholine release: effects of novelty, habituation, and fear. J Neurosci 1996, 16:3089-3096.
3. Andrieux A., Salin P.A., Vernet M., Kujala P., Baratier J., Gory-Fauré S., et al. The suppression of brain cold-stable microtubules in mice induces synaptic defects associated with neuroleptic-sensitive behavioral disorders. Genes Dev 2002, 16:2350-2364.
4. Apartis E., Poindessous-Jazat F.R., Lamour Y.A., Bassant M.H. Loss of rhythmically bursting neurons in rat medial septum following selective lesion of septohippocampal cholinergic system. J Neurophysiol 1998, 79:1633-1642.
5. Arendt T, Bigl V., Tennstedt A., Arendt A. Correlation between cortical plaque count and neuronal loss in the nucleus basalis in Alzheimer's disease. Neurosci Lett 1984, 48:81-85.
6. Armstrong D.M., Saper C.B., Levey A.I., Wainer B.H., Terry R.D. Distribution of cholinergic neurons in rat brain: demonstrated by the immunocytochemical localization of choline acetyltransferase. J Comp Neurol 1983, 216:53-68.
7. Azevedo F.A., Carvalho L.R., Grinberg L.T., Farfel J.M., Ferretti R.E., Leite R.E., et al. Equal numbers of neuronal and nonneuronal cells make the human brain an isometrically scaled-up primate brain. J Comp Neurol 2009, 513:532-541.
8. Baars B.J. Global workspace theory of consciousness: toward a cognitive neuroscience of human experience. Prog Brain Res 2005, 150:45-53.
9. Bamburg J.R., Bloom G.S. Cytoskeletal pathologies of Alzheimer disease. Cell Motil Cytoskeleton 2009, 66:635-649.
10. Barber R.P., Phelps P.E., Houser C.R., Crawford G.D., Salvaterra P.M., Vaughn J.E. The morphology and distribution of neurons containing choline acetyltransferase in the adult rat spinal cord: an immunocytochemical study. J Comp Neurol 1984, 229:329-346.
11. Bell G.A., Morgan I.G. The effects of colchicine and vinblastine on memory in chicks. Behav Brain Res 1981, 2:301-322.
12. Bensimon G., Chermat R. Microtubule disruption and cognitive defects: effect of colchicine on learning behavior in rats. Pharmacol Biochem Behav 1991, 38:141-145.
13. 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.
14. Birks J. Cholinesterase inhibitors for Alzheimer's disease. Cochrane Database Syst Rev 2006, 1:CD005593.
15. Björnström K., Eintrei C. The difference between sleep and anaesthesia is in the intracellular signal: propofol and GABA use different subtypes of the GABA(A) receptor beta subunit and vary in their interaction with actin. Acta Anaesthesiol Scand 2003, 47:157-164.
16. Blesch A., Tuszynski M.H. GDNF gene delivery to injured adult CNS motor neurons promotes axonal growth, expression of the trophic neuropeptide CGRP, and cellular protection. J Comp Neurol 2001, 436:399-410.
17. Bobkova N.V., Nesterova I.V., Nesterov V.V. The state of cholinergic structures in forebrain of bulbectomized mice. Bull Exp Biol Med 2001, 131:427-431.
18. Bondareff W. Synaptic atrophy in the senescent hippocampus. Mech Ageing Dev 1979, 9:163-171.
19. Bosch D., Schmid S. Cholinergic mechanism underlying prepulse inhibition of the startle response in rats. Neuroscience 2008, 155:326-335.
20. Boucetta S., Jones B.E. Activity profiles of cholinergic and intermingled GABAergic and putative glutamatergic neurons in the pontomesencephalic tegmentum of urethane-anesthetized rats. J Neurosci 2009, 29:4664-4674.
21. Bouvrais-Veret C., Weiss S., Andrieux A., Schweitzer A., McIntosh J.M., Job D., et al. Sustained increase of alpha7 nicotinic receptors and choline-induced improvement of learning deficit in STOP knock-out mice. Neuropharmacology 2007, 52:1691-1700.
22. Busetto G, Buffelli M., Cangiano L., Cangiano A. Effects of evoked and spontaneous motoneuronal firing on synapse competition and elimination in skeletal muscle. J Neurocytol 2003, 32:795-802.
23. Butcher L.L. Cholinergic neurons and networks. The rat nervous system: forebrain 1995, 1003-1015. Academic Press, Sydney. 2nd ed. G. Paxinos (Ed.).
24. Butcher L.L., Oh J.D., Woolf N.J. Cholinergic neurons identified by in situ hybridization histochemistry. Prog Brain Res 1993, 98:1-8.
25. Butcher L.L., Woolf N.J. Histochemical distribution of acetylcholinesterase in the central nervous system: clues to the localization of cholinergic neurons. Handbook of chemical neuroanatomy, volume 3: classical transmitters and transmitter receptors in the CNS, part II 1984, 1-50. Elsevier Biomedical Press, Amsterdam. A. Björklund, T. Hökfelt, M.J. Kuhar (Eds.).
26. Butcher L.L., Woolf N.J. Dysdifferentiation initiates and growth processes exacerbate the pathoogic cascade in Alzheimer's disease. Neurobiol Aging 1989, 10:557-570.
27. Butcher L.L., Woolf N.J. Cholinergic neurons and networks revisited. The rat central nervous system 2004, 1257-1268. Elsevier Academic Press, San Diego. 3rd ed. G. Paxinos (Ed.).
28. Cáceres A., Busciglio J., Ferreira A., Steward O. An immunocytochemical and biochemical study of the microtubule-associated protein MAP-2 during post-lesion dendritic remodeling in the central nervous system of adult rats. Brain Res 1988, 427:233-246.
29. Calaghan S.C., Le Guennec J.Y., White E. Cytoskeletal modulation of electrical and mechanical activity in cardiac myocytes. Prog Biophys Mol Biol 2004, 84:29-59.
30. Carlisle H.J., Kennedy M.B. Spine architecture and synaptic plasticity. Trends Neurosci 2005, 28:182-187.
31. Carter O.L., Pettigrew J.D. A common oscillator for perceptual rivalries?. Perception 2003, 32:295-305.
32. Cash A.D., Aliev G., Siedlak S.L., Nunomura A., Fujioka H., Zhu X., et al. Microtubule reduction in Alzheimer's disease and aging is independent of tau filament formation. Am J Pathol 2003, 162:1623-1627.
33. Chatzisotiriou A.S., Kapoukranidou D., Gougoulias N.E., Albani M. Effect of neonatal spinal transection and dorsal rhizotomy on hindlimb muscles. Dev Brain Res 2005, 157:113-123.
34. Chudasama Y., Dalley J.W., Nathwani F., Bouger P., Robbins T.W. Cholinergic modulation of visual attention and working memory: dissociable effects of basal forebrain 192-IgG-saporin lesions and intraprefrontal infusions of scopolamine. Learn Mem 2004, 11:78-86.
35. Clark E.W, Bernstein I.L. Boosting cholinergic activity in gustatory cortex enhances the salience of a familiar conditioned stimulus in taste aversion learning. Behav Neurosci 2009, 123:764-771.
36. Collerton D., Perry E., McKeith I. Why people see things that are not there: a novel perception and attention deficit model for recurrent complex visual hallucinations. Behav Brain Sci 2005, 28:737-757.
37. Conner J.M., Franks K.M., Titterness A.K., Russell K., Merrill D.A., Christie B.R., et al. NGF is essential for hippocampal plasticity and learning. J Neurosci 2009, 29:10883-10889.
38. Connolly J.A. Role of the cytoskeleton in the formation, stabilization, and removal of acetylcholine receptor clusters in cultured muscle cells. J Cell Biol 1984, 99:148-154.
39. Coronas V., Durand M., Chabot J.G., Jourdan F., Quirion R. Acetylcholine induces neuritic outgrowth in rat primary olfactory bulb cultures. Neuroscience 2000, 98:213-219.
40. Costa M.L., Escaleira R., Cataldo A., Oliveira F., Mermelstein C.S. Desmin: molecular interactions and putative functions of the muscle intermediate filament protein. Braz J Med Biol Res 2004, 37:1819-1830.
41. Crick F., Koch C. A framework for consciousness. Nat Neurosci 2003, 6:119-126.
42. Dean B., Boer S., Gibbons A., Money T., Scarr E. Recent advances in postmortem pathology and neurochemistry in schizophrenia. Curr Opin Psychiatry 2009, 22:154-160.
43. Deco G., Thiele A. Attention: oscillations and neuropharmacology. Eur J Neurosci 2009, 30:347-354.
44. Dietz V. Spinal cord pattern generators for locomotion. Clin Neurophysiol 2003, 114:1379-1389.
45. Derksen M.J., Ward N.L., Hartle K.D., Ivanco T.L. MAP2 and synaptophysin protein expression following motor learning suggests dynamic regulation and distinct alterations coinciding with synaptogenesis. Neurobiol Learn Mem 2007, 87:404-415.
46. Desplantez T., Dupont E., Severs N.J., Weingart R. Gap junction channels and cardiac impulse propagation. J Membr Biol 2007, 218:13-28.
47. Deutsch S.I., Rosse R.B., Lakshman R.M. Dysregulation of tau phosphorylation is a hypothesized point of convergence in the pathogenesis of Alzheimer's disease, frontotemporal dementia and schizophrenia with therapeutic implications. Prog Neuropsychopharmacol Biol Psychiatry 2006, 30:1369-1380.
48. Di Patre P.L., Oh J.D., Simmons J.M., Butcher L.L. Intrafimbrial colchicine produces transient impairment of radial-arm maze performance correlated with morphologic abnormalities of septohippocampal neurons expressing cholinergic markers and nerve growth factor receptor. Brain Res 1990, 523:316-320.
49. Dillon C., Goda Y. The actin cytoskeleton: integrating form and function at the synapse. Annu Rev Neurosci 2005, 28:25-55.
50. Dong H.L., Fukuda S., Murata E., Higuchi T. Excitatory and inhibitory actions of isoflurane on the cholinergic ascending arousal system of the rat. Anesthesiology 2006, 104:122-133.
51. Tononi G, Edelman G.M. Consciousness and complexity. Science 1998, 282:1846-1851.
52. Elvander-Tottie E., Eriksson T.M., Sandin J., Ogren S.O. 5-HT(1A) and NMDA receptors interact in the rat medial septum and modulate hippocampal-dependent spatial learning. Hippocampus 2009, 19:1187-1198.
53. Everitt B.J., Robbins T.W. Central cholinergic systems and cognition. Annu Rev Psychol 1997, 48:649-684.
54. Fadda F., Cocco S., Stancampiano R. Hippocampal acetylcholine release correlates with spatial learning performance in freely moving rats. Neuroreport 2000, 11:2265-2269.
55. Farris T.W, Woolf N.J., Oh J.D., Butcher L.L. Reestablishment of laminar patterns of cortical acetylcholinesterase activity following axotomy of the medial cholinergic pathway in the adult rat. Exp Neurol 1993, 121:77-92.
56. Farris T.W., Oh J.D., Butcher L.L., Woolf N.J. Trophic-factor modulation of cortical acetylcholinesterase reappearance following transection of the medial cholinergic pathway in adult rat. Exp Neurol 1995, 131:180-192.
57. Fischer A., Sananbenesi F., Schrick C., Spiess J., Radulovic J. Distinct roles of hippocampal de novo protein synthesis and actin rearrangement in extinction of contextual fear. J Neurosci 2004, 24:1962-1966.
58. Forlenza O.V., Spink J.M., Dayanandan R., Anderton B.H., Olesen O.F., Lovestone S. Muscarinic agonists reduce tau phosphorylation in non-neuronal cells via GSK-3beta inhibition and in neurons. J Neural Transm 2000, 107:1201-1212.
59. Franks N.P., Lieb W.R. Molecular and cellular mechanisms of general anaesthesia. Nature 1994, 367:607-614.
60. Fréchette M., Rennie K., Pappas B.A. Developmental forebrain cholinergic lesion and environmental enrichment: behaviour, CA1 cytoarchitecture and neurogenesis. Brain Res 2009, 1252:172-182.
61. Freeman W.J. A field-theoretic approach to understanding scale-free neocortical dynamics. Biol Cybern 2005, 92:350-359.
62. Fucile S. Ca2+ permeability of nicotinic acetylcholine receptors. Cell Calcium 2004, 35:1-8.
63. Fukamauchi F., Hough C., Chuang D.M. m2- and m3-muscarinic acetylcholine receptor mRNAs have different responses to microtubule-affecting drugs. Mol Cell Neurosci 1991, 2:315-319.
64. German D.C., Walker B.S., Manaye K., Smith W.K., Woodward D.J., North A.J. The human locus coeruleus: computer reconstruction of cellular distribution. J Neurosci 1988, 8:1776-1788.
65. Gordon A.M., Homsher E., Regnier M. Regulation of contraction in striated muscle. Physiol Rev 2000, 80:853-924.
66. Grillner S. The motor infrastructure: from ion channels to neuronal networks. Nat Rev Neurosci 2003, 4:573-586.
67. Grossberg S., Versace M. Spikes, synchrony, and attentive learning by laminar thalamocortical circuits. Brain Res 2008 Jul 7, 1218:278-312.
68. Haddad F., Roy R.R., Zhong H., Edgerton V.R., Baldwin K.M. Atrophy responses to muscle inactivity. II. Molecular markers of protein deficits. J Appl Physiol 2003, 95:791-802.
69. Harris K.M. Structure, development, and plasticity of dendritic spines. Curr Opin Neurobiol 1999, 9:343-348.
70. Houser C.R., Crawford G.D., Barber R.P., Salvaterra P.M., Vaughn J.E. Organization and morphological characteristics of cholinergic neurons: an immunocytochemical study with a monoclonal antibody to choline acetyltransferase. Brain Res 1983, 266:97-119.
71. Huxley H.E. Fifty years of muscle and the sliding filament hypothesis. Eur J Biochem 2004, 271:1403-1415.
72. Inglis W.L., Olmstead M.C., Robbins T.W. Selective deficits in attentional performance on the 5-choice serial reaction time task following pedunculopontine tegmental nucleus lesions. Behav Brain Res 2001, 123:117-131.
73. Iwata K., Yamamoto M., Nakao M., Kimura M. A study on polysomnographic observations and subjective experiences under sensory deprivation. Psychiatry Clin Neurosci 1999, 53:129-131.
74. Jaworski J., Kapitein L.C., Gouveia S.M., Dortland B.R., Wulf P.S., Grigoriev I., et al. Dynamic microtubules regulate dendritic spine morphology and synaptic plasticity. Neuron 2009, 61:85-100.
75. Jensen J.L., Marstrand P.C., Nielsen J.B. Motor skill training and strength training are associated with different plastic changes in the central nervous system. J Appl Physiol 2005, 99:1558-1568.
76. John E.R. A field theory of consciousness. Conscious Cogn 2001, 10:184-213.
77. John E.R. The neurophysics of consciousness. Brain Res Rev 2002, 39:1-28.
78. Johnson D.A., Zambon N.J., Gibbs R.B. Selective lesion of cholinergic neurons in the medial septum by 192 IgG-saporin impairs learning in a delayed matching to position T-maze paradigm. Brain Res 2002, 943:132-141.
79. Kaech S., Brinkhaus H., Matus A. Volatile anesthetics block actin-based motility in dendritic spines. Proc Natl Acad Sci USA 1999, 96:10433-10437.
80. Kaech S., Parmar H., Roelandse M., Bornmann C., Matus A. Cytoskeletal microdifferentiation: a mechanism for organizing morphological plasticity in dendrites. Proc Natl Acad Sci USA 2001, 98:7086-7092.
81. Keita M.S., Frankel-Kohn L., Bertrand N., Lecanu L., Monmaur P. Acetylcholine release in the hippocampus of the urethane anaesthetised rat positively correlates with both peak theta frequency and relative power in the theta band. Brain Res 2000, 887:323-334.
82. Khuchua Z., Wozniak D.F., Bardgett M.E., Yue Z., McDonald M., Boero J., et al. Deletion of the N-terminus of murine MAP2 by gene targeting disrupts hippocampal CA1 neuron architecture and alters contextual memory. Neuroscience 2003, 119:101-111.
83. Kimura H., McGeer P.L., Peng J.H., McGeer E.G. The central cholinergic system studied by choline acetyltransferase immunohistochemistry in the cat. J Comp Neurol 1981, 200(August (2)):151-201.
84. Kimura M., Yamada H., Matsumoto N. Tonically active neurons in the striatum encode motivational contexts of action. Brain Dev 2003, 25:S20-S23.
85. Kishino A., Ishige Y., Tatsuno T., Nakayama C., Noguchi H. BDNF prevents and reverses adult rat motor neuron degeneration and induces axonal outgrowth. Exp Neurol 1997, 144:273-286.
86. Kuo M.F., Grosch J., Fregni F., Paulus W., Nitsche M.A. Focusing effect of acetylcholine on neuroplasticity in the human motor cortex. J Neurosci 2007, 27:14442-14447.
87. Li W., Ochalski P.A., Brimijoin S., Jordan L.M., Nagy J.I. C-terminals on motoneurons: electron microscope localization of cholinergic markers in adult rats and antibody-induced depletion in neonates. Neuroscience 1995, 65:879-891.
88. Li Z., Mericskay M., Agbulut O., Butler-Browne G., Carlsson L., Thornell L.E., et al. Desmin is essential for the tensile strength and integrity of myofibrils but not for myogenic commitment, differentiation, and fusion of skeletal muscle. J Cell Biol 1997, 139:129-144.
89. Manaye K.F., Zweig R., Wu D., Hersh L.B., De Lacalle S., Saper C.B., et al. Quantification of cholinergic and select non-cholinergic mesopontine neuronal populations in the human brain. Neuroscience 1999, 89:759-770.
90. Meador K.J., Ray P.G., Echauz J.R., Loring D.W., Vachtsevanos G.J. Gamma coherence and conscious perception. Neurology 2002, 59:847-854.
91. Mena-Segovia J., Sims H.M., Magill P.J., Bolam J.P. Cholinergic brainstem neurons modulate cortical gamma activity during slow oscillations. J Physiol 2008, 586:2947-2960.
92. Mileusnic R., Lancashire C.L., Rose S.P. Recalling an aversive experience by day-old chicks is not dependent on somatic protein synthesis. Learn Mem 2005, 12:615-619.
93. Misawa H., Nakata K., Matsuura J., Nagao M., Okuda T., Haga T. Distribution of the high-affinity choline transporter in the central nervous system of the rat. Neuroscience 2001, 105:87-98.
94. Mitsui T., Kawajiri M., Kunishige M., Endo T., Akaike M., Aki K., et al. Functional association between nicotinic acetylcholine receptor and sarcomeric proteins via actin and desmin filaments. J Cell Biochem 2000, 77:584-595.
95. Mitsuyama F., Niimi G., Kato K., Hirosawa K., Mikoshiba K., Okuya M., et al. Redistribution of microtubules in dendrites of hippocampal CA1 neurons after tetanic stimulation during long-term potentiation. Ital J Anat Embryol 2008, 113:17-27.
96. Mohs R.C. The clinical syndrome of Alzheimer's disease: aspects particularly relevant to clinical trials. Genes Brain Behav 2005, 4:129-133.
97. Moos D.D. Central anticholinergic syndrome: a case report. J Perianesth Nurs 2007, 22:309-321.
98. Mori E., Hashimoto M., Krishnan K.R., Doraiswamy P.M. What constitutes clinical evidence for neuroprotection in Alzheimer disease: support for the cholinesterase inhibitors?. Alzheimer Dis Assoc Disord 2006, 20:S19-26.
99. Mufson E.J., Counts S.E., Perez S.E., Ginsberg S.D. Cholinergic system during the progression of Alzheimer's disease: therapeutic implications. Expert Rev Neurother 2008, 8:1703-1718.
100. Mufson E.J., Ma S.Y., Cochran E.J., Bennett D.A., Beckett L.A., Jaffar S., et al. Loss of nucleus basalis neurons containing TrkA immunoreactivity in individuals with mild cognitive impairment and early Alzheimer's disease. J Comp Neurol 2000, 427:19-30.
101. Myers C.P., Lewcock J.W., Hanson M.G., Gosgnach S., Aimone J.B., Gage F.H., et al. Cholinergic input is required during embryonic development to mediate proper assembly of spinal locomotor circuits. Neuron 2005, 46:37-49.
102. Nagai T., Kimura H., Maeda T., McGeer P.L., Peng F., McGeer E.G. Cholinergic projections from the basal forebrain of rat to the amygdala. J Neurosci 1982, 2:513-520.
103. Nail-Boucherie K., Dourmap N., Jaffard R., Costentin J. Contextual fear conditioning is associated with an increase of acetylcholine release in the hippocampus of rat. Cogn Brain Res 2000, 9:193-197.
104. Nakayama T., Sawada T. Involvement of microtubule integrity in memory impairment caused by colchicine. Pharmacol Biochem Behav 2002, 71:119-138.
105. Nelson T.J., Backlund P.S., Alkon D.L. Hippocampal protein-protein interactions in spatial memory. Hippocampus 2004, 14:46-57.
106. Niewiadomska G., Baksalerska-Pazera M., Riedel G. Cytoskeletal transport in the aging brain: focus on the cholinergic system. Rev Neurosci 2006, 17:581-618.
107. O'Connell C., O'Malley A., Regan C.M. Transient, learning-induced ultrastructural change in spatially-clustered dentate granule cells of the adult rat hippocampus. Neuroscience 1997, 76:55-62.
108. Pabion M., Job D., Margolis R.L. Sliding of STOP proteins on microtubules. Biochemistry 1984, 23:6642-6648.
109. Pákáski M., Kálmán J. Interactions between the amyloid and cholinergic mechanisms in Alzheimer's disease. Neurochem Int 2008, 53:103-111.
110. Pang K.C., Nocera R., Secor A.J., Yoder R.M. GABAergic septohippocampal neurons are not necessary for spatial memory. Hippocampus 2001, 11:814-827.
111. Parvizi J., Damasio A.R. Neuroanatomical correlates of brainstem coma. Brain 2003, 126:1524-1536.
112. Paxinos G., Bindra D. Rewarding intracranial stimulation, movement and the hippocampal theta rhythm. Physiol Behav 1970, 5:227-231.
113. Pearson A.M. Muscle growth and exercise. Crit Rev Food Sci Nutr 1990, 29:167-196.
114. Penschuck S., Chen-Bee C.H., Prakash N., Frostig R.D. In vivo modulation of a cortical functional sensory representation shortly after topical cholinergic agent application. J Comp Neurol 2002, 452:38-50.
115. Pepeu G., Giovannini M.G. Cholinesterase inhibitors and beyond. Curr Alzheimer Res 2009, 6:86-96.
116. Pesavento E., Capsoni S., Domenici L., Cattaneo A. Acute cholinergic rescue of synaptic plasticity in the neurodegenerating cortex of anti-nerve-growth-factor mice. Eur J Neurosci 2002, 15:1030-1036.
117. Phelps P.E., Houser C.R., Vaughn J.E. Immunocytochemical localization of choline acetyltransferase within the rat neostriatum: a correlated light and electron microscopic study of cholinergic neurons and synapses. J Comp Neurol 1985, 238:286-307.
118. Podolskii I.Y., Vorobev V.V., Belova N.A. Long-term changes in hippocampus and neocortex EEG spectra in response to pharmacological treatments affecting the cholinergic system. Neurosci Behav Physiol 2001, 31:589-595.
119. Powell K.J., Hori S.E., Leslie R., Andrieux A., Schellinck H., Thorne M., et al. Cognitive impairments in the STOP null mouse model of schizophrenia. Behav Neurosci 2007, 121:826-835.
120. Prives J., Fulton A.B., Penman S., Daniels M.P., Christian C.N. Interaction of the cytoskeletal framework with acetylcholine receptor on the surface of embryonic muscle cells in culture. J Cell Biol 1982, 92:231-236.
121. Rasmusson D.D. Cholinergic modulation of sensory information. Prog Brain Res 1993, 98:357-364.
122. Reep R.L., Corwin J.V. Posterior parietal cortex as part of a neural network for directed attention in rats. Neurobiol Learn Mem 2009, 91:104-113.
123. Roberts A., Perrins R. Positive feedback as a general mechanism for sustaining rhythmic and non-rhythmic activity. J Physiol Paris 1995, 89:241-248.
124. Ross R.G., Stevens K.E., Proctor W.R., Leonard S., Kisley M.A., Hunter S.K., et al. Research review: cholinergic mechanisms, early brain development, and risk for schizophrenia. J Child Psychol Psychiatry 2009, Nov 18, [epub].
125. Rostron C.L., Farquhar M.J., Latimer M.P., Winn P. The pedunculopontine tegmental nucleus and the nucleus basalis magnocellularis: do both have a role in sustained attention?. Neurol 2009, 513:532-541.
126. Roth A.L., Berg D.K. Large clusters of alpha7-containing nicotinic acetylcholine receptors on chick spinal cord neurons. J Comp Neurol 2003, 465:195-204.
127. Rubio A., Avila J., Pérez M. Effect of acetylcholine on tau phosphorylation in human neuroblastoma cells. J Mol Neurosci 2006, 30:185-188.
128. Ruediger T., Bolz J. Neurotransmitters and the development of neuronal circuits. Adv Exp Med Biol 2007, 621:104-115.
129. Rukhadze I., Kubin L. Mesopontine cholinergic projections to the hypoglossal motor nucleus. Neurosci Lett 2007, 413:121-125.
130. Ruthazer E.S. You're perfect, now change-redefining the role of developmental plasticity. Neuron 2005, 45:825-828.
131. Rye D.B., Saper C.B., Lee H.J., Wainer B.H. Pedunculopontine tegmental nucleus of the rat: cytoarchitecture, cytochemistry, and some extrapyramidal connections of the mesopontine tegmentum. J Comp Neurol 1987, 259:483-528.
132. Rye D.B., Wainer B.H., Mesulam M.M., Mufson E.J., 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 1984, 13:627-643.
133. Sadot E., Gurwitz D., Barg J., Behar L., Ginzburg I., Fisher A. Activation of m1 muscarinic acetylcholine receptor regulates tau phosphorylation in transfected PC12 cells. J Neurochem 1996, 66:877-880.
134. Saito A., Okano H., Bamba H., Hisa Y., Oomura Y., Imamura T., et al. Low expression of FGF1 (fibroblast growth factor-1) in rat parasympathetic preganglionic neurons. Histol Histopathol 2007, 22:1327-1335.
135. Sakai H., Kozutsumi Y., Goto K., Chiba Y., Misawa M. Functional importance of the cytoskeletal protein in acetylcholine-induced contraction of rat bronchial smooth muscle. J Smooth Muscle Res 2009, 45:97-108.
136. Sanders R.D., Brian D., Maze M. G-protein-coupled receptors. Handb Exp Pharmacol 2008, 182:93-117.
137. Saper C.B. Organization of cerebral cortical afferent systems in the rat. II. Magnocellular basal nucleus. J Comp Neurol 1984, 222:313-342.
138. Sarter M., Bruno J.P., Givens B. Attentional functions of cortical cholinergic inputs: what does it mean for learning and memory?. Neurobiol Learn Mem 2003, 80:245-256.
139. Schneck H.J., Rupreht J. Central anticholinergic syndrome (CAS) in anesthesia and intensive care. Acta Anaesthesiol Belg 1989, 40:219-228.
140. Semba K., Fibiger H.C. Organization of central cholinergic systems. Prog Brain Res 1989, 79:37-63.
141. Semba K., Fibiger H.C. Afferent connections of the laterodorsal and the pedunculopontine tegmental nuclei in the rat: a retro- and antero-grade transport and immunohistochemical study. J Comp Neurol 1992, 323:387-410.
142. Shapovalova K.B., Kamkina Y.V. Motor and cognitive functions of the neostriatum during bilateral blockade of its dopamine receptors. Neurosci Behav Physiol 2008, 38:71-79.
143. Shapalova K.B., Shuvaev V.T., Zhuravin I.A., Pominova E.V. Participation cholinergic systems of the dorsal and ventral striatum in the training of rats to avoidance in a T-maze. Neurosci Behav Physiol 1996, 26:288-294.
144. Shiromani P.J., Lai Y.Y., Siegel J.M. Descending projections from the dorsolateral pontine tegmentum to the paramedian reticular nucleus of the caudal medulla in the cat. Brain Res 1990, 517:224-228.
145. Siciliano R., Fornai F., Bonaccorsi I., Domenici L., Bagnoli P. Cholinergic and noradrenergic afferents influence the functional properties of the postnatal visual cortex in rats. Vis Neurosci 1999, 16:1015-1028.
146. Sigurdsson E.M. Tau-focused immunotherapy for Alzheimer's disease and related tauopathies. Curr Alzheimer Res 2009, 6:446-450.
147. Singer W. Consciousness and the binding problem. Ann N Y Acad Sci 2001, 929:123-146.
148. Sinkus M.L., Lee M.J., Gault J., Logel J., Short M., Freedman R., et al. A 2-base pair deletion polymorphism in the partial duplication of the alpha7 nicotinic acetylcholine gene (CHRFAM7A) on chromosome 15q14 is associated with schizophrenia. Brain Res 2009, 1291:1-11.
149. Sivaprakasam K. Towards a unifying hypothesis of Alzheimer's disease: cholinergic system linked to plaques, tangles and neuroinflammation. Curr Med Chem 2006, 13:2179-2188.
150. Smythies J. Philosophy, perception, and neuroscience. Perception 2009, 38:638-651.
151. Steriade M. Acetylcholine systems and rhythmic activities during the waking-sleep cycle. Prog Brain Res 2004, 145:179-196.
152. Steyn-Ross M.L., Steyn-Ross D.A., Sleigh J.W., Whiting D.R. Theoretical predictions for spatial covariance of the electroencephalographic signal during the anesthetic-induced phase transition: Increased correlation length and emergence of spatial self-organization. Phys Rev E 2003, 68:021902.
153. Sutherland R.J. The dorsal diencephalic conduction system: a review of the anatomy and functions of the habenular complex. Neurosci Biobehav Rev 1982, 6:1-13.
154. Szymusiak R., Alam N., McGinty D. Discharge patterns of neurons in cholinergic regions of the basal forebrain during waking and sleep. Behav Brain Res 2000, 115:171-182.
155. Talbot K., Woolf N.J., Butcher L.L. Feline islands of Calleja complex: II. Cholinergic and cholinesterasic features. J Comp Neurol 1988, 275:580-603.
156. Tandon R., Nasrallah H.A., Keshavan M.S. Schizophrenia, " just the facts" 4. Clinical features and conceptualization. Schizophr Res 2009, 110:1-23.
157. Taylor N.R., Hartley M., Taylor J.G. The micro-structure of attention. Neural Netw 2006, 19:1347-1370.
158. Torrão A.S., Lindstrom J.M., Britto L.R. Nicotine and alpha-bungarotoxin modify the dendritic growth of cholinoceptive neurons in the developing chick tectum. Dev Brain Res 2003, 143:115-118.
159. Valjakka A., Vartiainen J., Tuomisto L., Tuomisto J.T., Olkkonen H., Airaksinen M.M. The fasciculus retroflexus controls the integrity of REM sleep by supporting the generation of hippocampal theta rhythm and rapid eye movements in rats. Brain Res Bull 1998, 47:171-184.
160. Van der Zee E.A., Douma B.R., Bohus B., Luiten P.G. Passive avoidance training induces enhanced levels of immunoreactivity for muscarinic acetylcholine receptor and coexpressed PKC gamma and MAP-2 in rat cortical neurons. Cereb Cortex 1994, 4:376-390.
161. Van der Zee E.A., Luiten P.G. Muscarinic acetylcholine receptors in the hippocampus, neocortex and amygdala: a review of immunocytochemical localization in relation to learning and memory. Prog Neurobiol 1999, 58:409-471.
162. Van Dort C.J., Baghdoyan H.A., Lydic R. Neurochemical modulators of sleep and anesthetic states. Int Anesthesiol Clin 2008, 46:75-104.
163. Voytko M.L. Cognitive functions of the basal forebrain cholinergic system in monkeys: memory or attention?. Behav Brain Res 1996, 75:13-25.
164. Wainer B.H., Levey A.I., Rye D.B., Mesulam M.M., Mufson E.J. Cholinergic and non-cholinergic septohippocampal pathways. Neurosci Lett 1985, 54:45-52.
165. Walton J.R. Brain lesions comprised of aluminum-rich cells that lack microtubules may be associated with the cognitive deficit of Alzheimer's disease. Neurotoxicology 2009, 30:1059-1069.
166. Wang H.L., Morales M. Pedunculopontine and laterodorsal tegmental nuclei contain distinct populations of cholinergic, glutamatergic and GABAergic neurons in the rat. Eur J Neurosci 2009, 29:340-358.
167. Ward L.M. Synchronous neural oscillations and cognitive processes. Trends Cogn Sci 2003, 7:553-559.
168. Washbourne P., Liu X.B., Jones E.G., McAllister A.K. Cycling of NMDA receptors during trafficking in neurons before synapse formation. J Neurosci 2004, 24:8253-8264.
169. Weinberger N.M. Auditory associative memory and representational plasticity in the primary auditory cortex. Hear Res 2007, 229:54-68.
170. Wenk G.L. The nucleus basalis magnocellularis cholinergic system: one hundred years of progress. Neurobiol Learn Mem 1997, 67:85-95.
171. Wessler I. Acetylcholine release at motor endplates and autonomic neuroeffector junctions: a comparison. Pharmacol Res 1996, 33:81-94.
172. Whatley V.J., Harris R.A. The cytoskeleton and neurotransmitter receptors. Int Rev Neurobiol 1996, 39:113-143.
173. Woolf N.J. Cholinergic systems in mammalian brain and spinal cord. Prog Neurobiol 1991, 37:475-524.
174. Woolf N.J. A structural basis for memory storage in mammals. Prog Neurobiol 1998, 55:59-77.
175. Woolf N.J. Microtubules in the cerebral cortex: role in memory and consciousness. The emerging physics of consciousness 2006, Springer Verlag. J.A. Tuszynski (Ed.).
176. Woolf N.J. Acetylcholine, cognition, and consciousness. J Mol Neurosci 2006, 30:219-222.
177. Woolf N.J., Butcher L.L. Cholinergic neurons in the caudate-putamen complex proper are intrinsically organized: a combined Evans blue and acetylcholinesterase analysis. Brain Res Bull 1981, 7:487-507.
178. Woolf N.J., Butcher L.L. Cholinergic projections to the basolateral amygdala: a combined Evans Blue and acetylcholinesterase analysis. Brain Res Bull 1982, 8:751-763.
179. Woolf N.J., Butcher L.L. Cholinergic systems in the rat brain: III. Projections from the pontomesencephalic tegmentum to the thalamus, tectum, basal ganglia, and basal forebrain. Brain Res Bull 1986, 16:603-637.
180. Woolf N.J., Butcher L.L. Dysdifferentiation of structurally plastic neurons initiates the pathologic cascade of Alzheimer's disease: toward a unifying hypothesis. Cholinergic systems 1990, 387-438. Oxford University Press, New York. M. Steriade, D. Biesold (Eds.).
181. Woolf N.J., Eckenstein F., Butcher L.L. Cholinergic systems in the rat brain: I. projections to the limbic telencephalon. Brain Res Bull 1984, 13:751-784.
182. Woolf N.J., Milov A.M., Schweitzer E.S., Roghani A. Elevation of nerve growth factor and antisense knockdown of TrkA receptor during contextual memory consolidation. J Neurosci 2001, 21:1047-1055.
183. Woolf N.J., Young S.L., Johnson G.V., Fanselow M.S. Pavlovian conditioning alters cortical microtubule-associated protein-2. Neuroreport 1994, 5:1045-1048.
184. Woolf N.J., Zinnerman M.D., Johnson G.V. Hippocampal microtubule-associated protein-2 alterations with contextual memory. Brain Res 1999, 821:241-249.
185. Yamaguchi S., Fujii-Taira I., Murakami A., Hirose N., Aoki N., Izawa E., et al. Up-regulation of microtubule-associated protein2 accompanying the filial imprinting of domestic chicks (Gallus gallus domesticus). Brain Res Bull 2008, 76:282-288.
186. Yuen E.Y., Jiang Q., Feng J., Yan Z. Microtubule regulation of N-methyl-d-aspartate receptor channels in neurons. J Biol Chem 2005, 280:29420-29427.
187. Zacksenhouse M. Sensitivity of basic oscillatory mechanisms for pattern generation and detection. Biol Cybern 2001, 85:301-311.
188. Zubek J.P. Effects of prolonged sensory and perceptual deprivation. Br Med Bull 1964, 20:38-42.