Cholinergic Circuits and Signaling in the Pathophysiology of Schizophrenia

International Review of Neurobiology

Volumn 78, Issue , 2007, Pages 193-223

  Berman, Joshua A ^a   Talmage, David A ^a   Role, Lorna W ^a  

^a New York State Psychiatric Institute ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCHOLINE; CHOLINERGIC RECEPTOR; NEUROLEPTIC AGENT;

ANIMAL; BRAIN; CHOLINERGIC NERVE; DRUG EFFECT; HUMAN; METABOLISM; NERVE TRACT; PATHOPHYSIOLOGY; PHYSIOLOGY; REVIEW; SCHIZOPHRENIA; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION;

ACETYLCHOLINE; ANIMALS; ANTIPSYCHOTIC AGENTS; BRAIN; CHOLINERGIC FIBERS; HUMANS; NEURAL PATHWAYS; RECEPTORS, CHOLINERGIC; SCHIZOPHRENIA; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION;

EID: 33847624671     PISSN: 00747742     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0074-7742(06)78007-2     Document Type: Review

References (157)

1. Aasen I., Kumari V., and Sharma T. Effects of rivastigmine on sustained attention in schizophrenia: An FMRI study. J. Clin. Psychopharmacol. 25 (2005) 311-317
2. Albuquerque E.X., Pereira E.F., Bonfante-Cabarcas R., Marchioro M., Matsubayashi H., Alkondon M., and Maelicke A. Nicotinic acetylcholine receptors on hippocampal neurons: Cell compartment-specific expression and modulatory control of channel activity. Prog. Brain Res. 109 (1996) 111-124
3. Apicella P. Tonically active neurons in the primate striatum and their role in the processing of information about motivationally relevant events. Eur. J. Neurosci. 16 (2002) 2017-2026
4. Avila M.T., Sherr J.D., Hong E., Myers C.S., and Thaker G.K. Effects of nicotine on leading saccades during smooth pursuit eye movements in smokers and nonsmokers with schizophrenia. Neuropsychopharmacology 28 (2003) 2184-2191
5. Aznavour N., Watkins K.C., and Descarries L. Postnatal development of the cholinergic innervation in the dorsal hippocampus of rat: Quantitative light and electron microscopic immunocytochemical study. J. Comp. Neurol. 486 (2005) 61-75
6. Bachy I., and Retaux S. GABAergic specification in the basal forebrain is controlled by the LIM-hd factor Lhx7. Dev. Biol. 291 (2006) 218-226
7. Berger-Sweeney J. The cholinergic basal forebrain system during development and its influence on cognitive processes: Important questions and potential answers. Neurosci. Biobehav. Rev. 27 (2003) 401-411
8. Borda T., Perez Rivera R., Joensen L., Gomez R.M., and Sterin-Borda L. Antibodies against cerebral M1 cholinergic muscarinic receptor from schizophrenic patients: Molecular interaction. J. Immunol. 168 (2002) 3667-3674
9. Brady D.R., Phelps P.E., and Vaughn J.E. Neurogenesis of basal forebrain cholinergic neurons in rat. Brain Res. Dev. Brain Res. 47 (1989) 81-92
10. Brebion G., Bressan R.A., Amador X., Malaspina D., and Gorman J.M. Medications and verbal memory impairment in schizophrenia: The role of anticholinergic drugs. Psychol. Med. 34 (2004) 369-374
11. Breese C.R., Lee M.J., Adams C.E., Sullivan B., Logel J., Gillen K.M., Marks M.J., Collins A.C., and Leonard S. Abnormal regulation of high affinity nicotinic receptors in subjects with schizophrenia. Neuropsychopharmacology 23 (2000) 351-364
12. Bresnahan M., Schaefer C.A., Brown A.S., and Susser E.S. Prenatal determinants of schizophrenia: What we have learned thus far?. Epidemiol. Psichiatr. Soc. 14 (2005) 194-197
13. Buzsaki G. Theta oscillations in the hippocampus. Neuron 33 (2002) 325-340
14. Bymaster F.P., Calligaro D.O., Falcone J.F., Marsh R.D., Moore N.A., Tye N.C., Seeman P., and Wong D.T. Radioreceptor binding profile of the atypical antipsychotic olanzapine. Neuropsychopharmacology 14 (1996) 87-96
15. Bymaster F.P., Shannon H.E., Rasmussen K., DeLapp N.W., Ward J.S., Calligaro D.O., Mitch C.H., Whitesitt C., Ludvigsen T.S., Sheardown M., Swedberg M., Rasmussen T., et al. Potential role of muscarinic receptors in schizophrenia. Life Sci. 64 (1999) 527-534
16. Bymaster F.P., Felder C., Ahmed S., and McKinzie D. Muscarinic receptors as a target for drugs treating schizophrenia. Curr. Drug. Targets CNS Neurol. Disord. 1 (2002) 163-181
17. Bymaster F.P., Felder C.C., Tzavara E., Nomikos G.G., Calligaro D.O., and McKinzie D.L. Muscarinic mechanisms of antipsychotic atypicality. Prog. Neuropsychopharmacol. Biol. Psychiatry 27 (2003) 1125-1143
18. Calabresi P., Centonze D., Gubellini P., Pisani A., and Bernardi G. Acetylcholine-mediated modulation of striatal function. Trends Neurosci. 23 (2000) 120-126
19. Clancy B., Darlington R.B., and Finlay B.L. Translating developmental time across mammalian species. Neuroscience 105 (2001) 7-17
20. Cobb S.R., and Davies C.H. Cholinergic modulation of hippocampal cells and circuits. J. Physiol. 562 (2005) 81-88
21. Colgin L.L., Kramar E.A., Gall C.M., and Lynch G. Septal modulation of excitatory transmission in hippocampus. J. Neurophysiol. 90 (2003) 2358-2366
22. Corcoran C., Gallitano A., Leitman D., and Malaspina D. The neurobiology of the stress cascade and its potential relevance for schizophrenia. J. Psychiatr. Pract. 7 (2001) 3-14
23. Corcoran C., Walker E., Huot R., Mittal V., Tessner K., Kestler L., and Malaspina D. The stress cascade and schizophrenia: Etiology and onset. Schizophr. Bull. 29 (2003) 671-692
24. Court J., Spurden D., Lloyd S., McKeith I., Ballard C., Cairns N., Kerwin R., Perry R., and Perry E. Neuronal nicotinic receptors in dementia with Lewy bodies and schizophrenia: Alpha-bungarotoxin and nicotine binding in the thalamus. J. Neurochem. 73 (1999) 1590-1597
25. Court J.A., Piggott M.A., Lloyd S., Cookson N., Ballard C.G., McKeith I.G., Perry R.H., and Perry E.K. Nicotine binding in human striatum: Elevation in schizophrenia and reductions in dementia with Lewy bodies, Parkinson's disease and Alzheimer's disease and in relation to neuroleptic medication. Neuroscience 98 (2000) 79-87
26. Coyle J., and Kershaw P. Galantamine, a cholinesterase inhibitor that allosterically modulates nicotinic receptors: Effects on the course of Alzheimer's disease. Biol. Psychiatry 49 (2001) 289-299
27. Cragg S.J. Meaningful silences: How dopamine listens to the ACh pause. Trends Neurosci. 29 (2006) 125-131
28. Crismon M.L. Tacrine: First drug approved for Alzheimer's disease. Ann. Pharmacother. 28 (1994) 744-751
29. Crook J.M., Tomaskovic-Crook E., Copolov D.L., and Dean B. Decreased muscarinic receptor binding in subjects with schizophrenia: A study of the human hippocampal formation. Biol. Psychiatry 48 (2000) 381-388
30. Dalack G.W., Becks L., Hill E., Pomerleau O.F., and Meador-Woodruff J.H. Nicotine withdrawal and psychiatric symptoms in cigarette smokers with schizophrenia. Neuropsychopharmacology 21 (1999) 195-202
31. De Luca V., Wong A.H., Muller D.J., Wong G.W., Tyndale R.F., and Kennedy J.L. Evidence of association between smoking and alpha7 nicotinic receptor subunit gene in schizophrenia patients. Neuropsychopharmacology 29 (2004) 1522-1526
32. Dean B., Crook J.M., Pavey G., Opeskin K., and Copolov D.L. Muscarinic1 and 2 receptor mRNA in the human caudate-putamen: No change in m1 mRNA in schizophrenia. Mol. Psychiatry 5 (2000) 203-207
33. Dean B., McLeod M., Keriakous D., McKenzie J., and Scarr E. Decreased muscarinic1 receptors in the dorsolateral prefrontal cortex of subjects with schizophrenia. Mol. Psychiatry 7 (2002) 1083-1091
34. DeBoer P., Heeringa M.J., and Abercrombie E.D. Spontaneous release of acetylcholine in striatum is preferentially regulated by inhibitory dopamine D2 receptors. Eur. J. Pharmacol. 317 (1996) 257-262
35. Depatie L., O'Driscoll G.A., Holahan A.L., Atkinson V., Thavundayil J.X., Kin N.N., and Lal S. Nicotine and behavioral markers of risk for schizophrenia: A double-blind, placebo-controlled, cross-over study. Neuropsychopharmacology 27 (2002) 1056-1070
36. Dooley M., and Lamb H.M. Donepezil: A review of its use in Alzheimer's disease. Drugs Aging 16 (2000) 199-226
37. Eriksson P., Ankarberg E., Viberg H., and Fredriksson A. The developing cholinergic system as target for environmental toxicants, nicotine and polychlorinated biphenyls (PCBs): Implications for neurotoxicological processes in mice. Neurotox. Res. 3 (2001) 37-51
38. Fagan A.M., Garber M., Barbacid M., Silos-Santiago I., and Holtzman D.M. A role for TrkA during maturation of striatal and basal forebrain cholinergic neurons in vivo. J. Neurosci. 17 (1997) 7644-7654
39. Falls D.L., Rosen K.M., Corfas G., Lane W.S., and Fischbach G.D. ARIA, a protein that stimulates acetylcholine receptor synthesis, is a member of the neu ligand family. Cell 72 (1993) 801-815
40. Flames N., Long J.E., Garratt A.N., Fischer T.M., Gassmann M., Birchmeier C., Lai C., Rubenstein J.L., and Marin O. Short- and long-range attraction of cortical GABAergic interneurons by neuregulin-1. Neuron 44 (2004) 251-261
41. Frazier C.J., Rollins Y.D., Breese C.R., Leonard S., Freedman R., and Dunwiddie T.V. Acetylcholine activates an alpha-bungarotoxin-sensitive nicotinic current in rat hippocampal interneurons, but not pyramidal cells. J. Neurosci. 18 (1998) 1187-1195
42. Freedman R., Olincy A., Ross R.G., Waldo M.C., Stevens K.E., Adler L.E., and Leonard S. The genetics of sensory gating deficits in schizophrenia. Curr. Psychiatry Rep. 5 (2003) 155-161
43. Friedman J.I., Adler D.N., Howanitz E., Harvey P.D., Brenner G., Temporini H., White L., Parrella M., and Davis K.L. A double blind placebo controlled trial of donepezil adjunctive treatment to risperidone for the cognitive impairment of schizophrenia. Biol. Psychiatry 51 (2002) 349-357
44. Furusho M., Ono K., Takebayashi H., Masahira N., Kagawa T., Ikeda K., and Ikenaka K. Involvement of the Olig2 transcription factor in cholinergic neuron development of the basal forebrain. Dev. Biol. 293 (2006) 348-357
45. Gotti C., and Clementi F. Neuronal nicotinic receptors: From structure to pathology. Prog. Neurobiol. 74 (2004) 363-396
46. Graybiel A.M., Aosaki T., Flaherty A.W., and Kimura M. The basal ganglia and adaptive motor control. Science 265 (1994) 1826-1831
47. Grosse G., Djalali S., Deng D.R., Holtje M., Hinz B., Schwartzkopff K., Cygon M., Rothe T., Stroh T., Hellweg R., Ahnert-Hilger G., and Hortnag H. Area-specific effects of brain-derived neurotrophic factor (BDNF) genetic ablation on various neuronal subtypes of the mouse brain. Brain Res. Dev. Brain Res. 156 (2005) 111-126
48. Guijarro C., Rutz S., Rothmaier K., Turiault M., Zhi Q., Naumann T., Frotscher M., Tronche F., Jackisch R., and Kretz O. Maturation and maintenance of cholinergic medial septum neurons require glucocorticoid receptor signaling. J. Neurochem. 97 (2006) 747-758
49. Haroutunian V., Davidson M., Kanof P.D., Perl D.P., Powchik P., Losonczy M., McCrystal J., Purohit D.P., Bierer L.M., and Davis K.L. Cortical cholinergic markers in schizophrenia. Schizophr. Res. 12 (1994) 137-144
50. Harrison P.J., and Weinberger D.R. Schizophrenia genes, gene expression, and neuropathology: On the matter of their convergence. Mol. Psychiatry 10 (2005) 40-68 ; image 5
51. Hasselmo M.E. What is the function of hippocampal theta rhythm?-Linking behavioral data to phasic properties of field potential and unit recording data. Hippocampus 15 (2005) 936-949
52. Hohmann C.F. A morphogenetic role for acetylcholine in mouse cerebral neocortex. Neurosci. Biobehav. Rev. 27 (2003) 351-363
53. Hohmann C.F., and Berger-Sweeney J. Cholinergic regulation of cortical development and plasticity. New twists to an old story. Perspect. Dev. Neurobiol. 5 (1998) 401-425
54. Holt D.J., Herman M.M., Hyde T.M., Kleinman J.E., Sinton C.M., German D.C., Hersh L.B., Graybiel A.M., and Saper C.B. Evidence for a deficit in cholinergic interneurons in the striatum in schizophrenia. Neuroscience 94 (1999) 21-31
55. Holt D.J., Bachus S.E., Hyde T.M., Wittie M., Herman M.M., Vangel M., Saper C.B., and Kleinman J.E. Reduced density of cholinergic interneurons in the ventral striatum in schizophrenia: An in situ hybridization study. Biol. Psychiatry 58 (2005) 408-416
56. Hyde T.M., and Crook J.M. Cholinergic systems and schizophrenia: Primary pathology or epiphenomena?. J. Chem. Neuroanat. 22 (2001) 53-63
57. Ichikawa J., Dai J., O'Laughlin I.A., Fowler W.L., and Meltzer H.Y. Atypical, but not typical, antipsychotic drugs increase cortical acetylcholine release without an effect in the nucleus accumbens or striatum. Neuropsychopharmacology 26 (2002) 325-339
58. Jacobsen L.K., D'Souza D.C., Mencl W.E., Pugh K.R., Skudlarski P., and Krystal J.H. Nicotine effects on brain function and functional connectivity in schizophrenia. Biol. Psychiatry 55 (2004) 850-888
59. Jann M.W. Rivastigmine, a new-generation cholinesterase inhibitor for the treatment of Alzheimer's disease. Pharmacotherapy 20 (2000) 1-12
60. Ji D., Lape R., and Dani J.A. Timing and location of nicotinic activity enhances or depresses hippocampal synaptic plasticity. Neuron 31 (2001) 131-141
61. Johnson D.E., Nedza F.M., Spracklin D.K., Ward K.M., Schmidt A.W., Iredale P.A., Godek D.M., and Rollema H. The role of muscarinic receptor antagonism in antipsychotic-induced hippocampal acetylcholine release. Eur. J. Pharmacol. 506 (2005) 209-219
62. Johnston M.V., Rutkowski J.L., Wainer B.H., Long J.B., and Mobley W.C. NGF effects on developing forebrain cholinergic neurons are regionally specific. Neurochem. Res. 12 (1987) 985-994
63. Johnstone E.C., Crow T.J., Ferrier I.N., Frith C.D., Owens D.G., Bourne R.C., and Gamble S.J. Adverse effects of anticholinergic medication on positive schizophrenic symptoms. Psychol. Med. 13 (1983) 513-527
64. Jones S., and Yakel J.L. Functional nicotinic ACh receptors on interneurones in the rat hippocampus. J. Physiol. 504 Pt. 3 (1997) 603-610
65. Kane J., Honigfeld G., Singer J., and Meltzer H. Clozapine for the treatment-resistant schizophrenic. A double-blind comparison with chlorpromazine. Arch. Gen. Psychiatry 45 (1988) 789-796
66. Kane J.M., Marder S.R., Schooler N.R., Wirshing W.C., Umbricht D., Baker R.W., Wirshing D.A., Safferman A., Ganguli R., McMeniman M., and Borenstein M. Clozapine and haloperidol in moderately refractory schizophrenia: A 6-month randomized and double-blind comparison. Arch. Gen. Psychiatry 58 (2001) 965-972
67. Kawai H., Zago W., and Berg D.K. Nicotinic alpha 7 receptor clusters on hippocampal GABAergic neurons: Regulation by synaptic activity and neurotrophins. J. Neurosci. 22 (2002) 7903-7912
68. Laplante F., Srivastava L.K., and Quirion R. Alterations in dopaminergic modulation of prefrontal cortical acetylcholine release in post-pubertal rats with neonatal ventral hippocampal lesions. J. Neurochem. 89 (2004) 314-323
69. Larrison-Faucher A.L., Matorin A.A., and Sereno A.B. Nicotine reduces antisaccade errors in task impaired schizophrenic subjects. Prog. Neuropsychopharmacol. Biol. Psychiatry 28 (2004) 505-516
70. Laviolette S.R., and van der Kooy D. The neurobiology of nicotine addiction: Bridging the gap from molecules to behaviour. Nat. Rev. Neurosci. 5 (2004) 55-65
71. Lee M.G., Hassani O.K., Alonso A., and Jones B.E. Cholinergic basal forebrain neurons burst with theta during waking and paradoxical sleep. J. Neurosci. 25 (2005) 4365-4369
72. Lenzi A., Maltinti E., Poggi E., Fabrizio L., and Coli E. Effects of rivastigmine on cognitive function and quality of life in patients with schizophrenia. Clin. Neuropharmacol. 26 (2003) 317-321
73. Leonard S., Adams C., Breese C.R., Adler L.E., Bickford P., Byerley W., Coon H., Griffith J.M., Miller C., Myles-Worsley M., Nagamoto H.T., Rollins Y., et al. Nicotinic receptor function in schizophrenia. Schizophr. Bull. 22 (1996) 431-445
74. Leonard S., Gault J., Hopkins J., Logel J., Vianzon R., Short M., Drebing C., Berger R., Venn D., Sirota P., Zerbe G., Olincy A., et al. Association of promoter variants in the alpha7 nicotinic acetylcholine receptor subunit gene with an inhibitory deficit found in schizophrenia. Arch. Gen. Psychiatry 59 (2002) 1085-1096
75. Levin E.D., Wilson W., Rose J.E., and McEvoy J. Nicotine-haloperidol interactions and cognitive performance in schizophrenics. Neuropsychopharmacology 15 (1996) 429-436
76. Levin E.D., McClernon F.J., and Rezvani A.H. Nicotinic effects on cognitive function: Behavioral characterization, pharmacological specification, and anatomic localization. Psychopharmacology (Berl.) 184 (2006) 523-539
77. Lewis D.A. The organization of chemically-identified neural systems in monkey prefrontal cortex: Afferent systems. Prog. Neuropsychopharmacol. Biol. Psychiatry 14 (1990) 371-377
78. Li Z., Huang M., Ichikawa J., Dai J., and Meltzer H.Y. N-desmethylclozapine, a major metabolite of clozapine, increases cortical acetylcholine and dopamine release in vivo via stimulation of M1 muscarinic receptors. Neuropsychopharmacology 30 (2005) 1986-1995
79. Liao D.L., Hong C.J., Chen H.M., Chen Y.E., Lee S.M., Chang C.Y., Chen H., and Tsai S.J. Association of muscarinic m1 receptor genetic polymorphisms with psychiatric symptoms and cognitive function in schizophrenic patients. Neuropsychobiology 48 (2003) 72-76
80. Lieberman J.A., Phillips M., Gu H., Stroup S., Zhang P., Kong L., Ji Z., Koch G., and Hamer R.M. Atypical and conventional antipsychotic drugs in treatment-naive first-episode schizophrenia: A 52-week randomized trial of clozapine vs chlorpromazine. Neuropsychopharmacology 28 (2003) 995-1003
81. Lieberman J.A., Stroup T.S., McEvoy J.P., Swartz M.S., Rosenheck R.A., Perkins D.O., Keefe R.S., Davis S.M., Davis C.E., Lebowitz B.D., Severe J., and Hsiao J.K. Effectiveness of antipsychotic drugs in patients with chronic schizophrenia. N. Engl. J. Med. 353 (2005) 1209-1223
82. Liu Y., Ford B., Mann M.A., and Fischbach G.D. Neuregulins increase alpha7 nicotinic acetylcholine receptors and enhance excitatory synaptic transmission in GABAergic interneurons of the hippocampus. J. Neurosci. 21 (2001) 5660-5669
83. Lopez-Bendito G., Cautinat A., Sanchez J.A., Bielle F., Flames N., Garratt A.N., Talmage D.A., Role L.W., Charnay P., Marin O., and Garel S. Tangential neuronal migration controls axon guidance: A role for neuregulin-1 in thalamocortical axon navigation. Cell 125 (2006) 127-142
84. Lucas-Meunier E., Fossier P., Baux G., and Amar M. Cholinergic modulation of the cortical neuronal network. Pflugers Arch. 446 (2003) 17-29
85. MacDermott A.B., Role L.W., and Siegelbaum S.A. Presynaptic ionotropic receptors and the control of transmitter release. Annu. Rev. Neurosci. 22 (1999) 443-485
86. Mansvelder H.D., van Aerde K.I., Couey J.J., and Brussaard A.B. Nicotinic modu- lation of neuronal networks: From receptors to cognition. Psychopharmacology (Berl) 184 (2006) 292-305
87. Marin O., Anderson S.A., and Rubenstein J.L. Origin and molecular specification of striatal interneurons. J. Neurosci. 20 (2000) 6063-6076
88. + channels reduces autonomous activity in striatal cholinergic interneurons. J. Neurosci. 24 (2004) 10289-10301
89. Mazeh D., Zemishlani H., Barak Y., Mirecki I., and Paleacu D. Donepezil for negative signs in elderly patients with schizophrenia: An add-on, double-blind, crossover, placebo-controlled study. Int. Psychogeriatr. 18 3 (2006) 429-436
90. McEvoy J.P., and Freter S. The dose-response relationship for memory impairment by anticholinergic drugs. Compr. Psychiatry 30 (1989) 135-138
91. Mechawar N., and Descarries L. The cholinergic innervation develops early and rapidly in the rat cerebral cortex: A quantitative immunocytochemical study. Neuroscience 108 (2001) 555-567
92. Mendelsohn E., Rosenthal M., Bohiri Y., Werber E., Kotler M., and Strous R.D. Rivastigmine augmentation in the management of chronic schizophrenia with comorbid dementia: An open-label study investigating effects on cognition, behaviour and activities of daily living. Int. Clin. Psychopharmacol. 19 (2004) 319-324
93. Mesulam M.M. Spatial attention and neglect: Parietal, frontal and cingulate contributions to the mental representation and attentional targeting of salient extrapersonal events. Philos. Trans R. Soc. Lond. B Biol. Sci. 354 (1999) 1325-1346
94. Mesulam M.M. The cholinergic innervation of the human cerebral cortex. Prog. Brain Res. 145 (2004) 67-78
95. Mesulam M.M., Mufson E.J., Levey A.I., and Wainer B.H. Atlas of cholinergic neurons in the forebrain and upper brainstem of the macaque based on monoclonal choline acetyltransferase immunohistochemistry and acetylcholinesterase histochemistry. Neuroscience 12 (1984) 669-686
96. Michal P., Lysikova M., El-Fakahany E.E., and Tucek S. Clozapine interaction with the M2 and M4 subtypes of muscarinic receptors. Eur. J. Pharmacol. 376 (1999) 119-125
97. Mirza N.R., Peters D., and Sparks R.G. Xanomeline and the antipsychotic potential of muscarinic receptor subtype selective agonists. CNS Drug Rev. 9 (2003) 159-186
98. Mobley W.C., Rutkowski J.L., Tennekoon G.I., Gemski J., Buchanan K., and Johnston M.V. Nerve growth factor increases choline acetyltransferase activity in developing basal forebrain neurons. Brain Res. 387 (1986) 53-62
99. Moore H., Fadel J., Sarter M., and Bruno J.P. Role of accumbens and cortical dopamine receptors in the regulation of cortical acetylcholine release. Neuroscience 88 (1999) 811-822
100. Mori T., Yuxing Z., Takaki H., Takeuchi M., Iseki K., Hagino S., Kitanaka J., Takemura M., Misawa H., Ikawa M., Okabe M., and Wanaka A. The LIM homeobox gene, L3/Lhx8, is necessary for proper development of basal forebrain cholinergic neurons. Eur. J. Neurosci. 19 (2004) 3129-3141
101. Myers C.S., Robles O., Kakoyannis A.N., Sherr J.D., Avila M.T., Blaxton T.A., and Thaker G.K. Nicotine improves delayed recognition in schizophrenic patients. Psychopharmacology (Berl.) 174 (2004) 334-340
102. Nahas Z., George M.S., Horner M.D., Markowitz J.S., Li X., Lorberbaum J.P., Owens S.D., McGurk S., DeVane L., and Risch S.C. Augmenting atypical antipsychotics with a cognitive enhancer (donepezil) improves regional brain activity in schizophrenia patients: A pilot double-blind placebo controlled BOLD fMRI study. Neurocase 9 (2003) 274-282
103. Newhouse P.A., Potter A., and Singh A. Effects of nicotinic stimulation on cognitive performance. Curr. Opin. Pharmacol. 4 (2004) 36-46
104. Ninan I., and Kulkarni S.K. Clozapine-induced cognitive dysfunction in mice. Methods Find. Exp. Clin. Pharmacol. 18 (1996) 367-372
105. Olsson M., Bjorklund A., and Campbell K. Early specification of striatal projection neurons and interneuronal subtypes in the lateral and medial ganglionic eminence. Neuroscience 84 (1998) 867-876
106. Parikh V., Evans D.R., Khan M.M., and Mahadik S.P. Nerve growth factor in never-medicated first-episode psychotic and medicated chronic schizophrenic patients: Possible implications for treatment outcome. Schizophr. Res. 60 (2003) 117-123
107. Park S., Knopick C., McGurk S., and Meltzer H.Y. Nicotine impairs spatial working memory while leaving spatial attention intact. Neuropsychopharmacology 22 (2000) 200-209
108. Partridge J.G., Apparsundaram S., Gerhardt G.A., Ronesi J., and Lovinger D.M. Nicotinic acetylcholine receptors interact with dopamine in induction of striatal long term depression. J. Neurosci. 22 (2002) 2541-2549
109. Phillips H.S., Nishimura M., Armanini M.P., Chen K., Albers K.M., and Davis B.M. Rescue of NGF-deficient mice II: Basal forebrain cholinergic projections require NGF for target innervation but not guidance. Brain Res. Mol. Brain Res. 124 (2004) 1-11
110. Picciotto M.R. Nicotine as a modulator of behavior: Beyond the inverted U. Trends Pharmacol. Sci. 24 (2003) 493-499
111. Raedler T.J., Knable M.B., Jones D.W., Urbina R.A., Gorey J.G., Lee K.S., Egan M.F., Coppola R., and Weinberger D.R. In vivo determination of muscarinic acetylcholine receptor availability in schizophrenia. Am. J. Psychiatry 160 (2003) 118-127
112. Reddy G.R., Basha M.R., Devi C.B., Suresh A., Baker J.L., Shafeek A., Heinz J., and Chetty C.S. Lead induced effects on acetylcholinesterase activity in cerebellum and hippocampus of developing rat. Int. J. Dev. Neurosci. 21 (2003) 347-352
113. Rice M.E., and Cragg S.J. Nicotine amplifies reward-related dopamine signals in striatum. Nat. Neurosci. 7 (2004) 583-584
114. Robinson S.E. Effects of perinatal buprenorphine and methadone exposures on striatal cholinergic ontogeny. Neurotoxicol. Teratol. 24 (2002) 137-142
115. Role L.W., and Berg D.K. Nicotinic receptors in the development and modulation of CNS synapses. Neuron 16 (1996) 1077-1085
116. Rosse R.B., and Deutsch S.I. Adjuvant galantamine administration improves negative symptoms in a patient with treatment-refractory schizophrenia. Clin. Neuropharmacol. 25 (2002) 272-275
117. Sacco K.A., Bannon K.L., and George T.P. Nicotinic receptor mechanisms and cognition in normal states and neuropsychiatric disorders. J. Psychopharmacol. 18 (2004) 457-474
118. Sarter M., and Parikh V. Choline transporters, cholinergic transmission and cognition. Nat. Rev. Neurosci. 6 (2005) 48-56
119. Sarter M., Nelson C.L., and Bruno J.P. Cortical cholinergic transmission and cortical information processing in schizophrenia. Schizophr. Bull. 31 (2005) 117-138
120. Scarr E., Keriakous D., Crossland N., and Dean B. No change in cortical muscarinic M2, M3 receptors or [35S]GTPgammaS binding in schizophrenia. Life Sci. 78 (2006) 1231-1237
121. Semba K., Vincent S.R., and Fibiger H.C. Different times of origin of choline acetyltransferase- and somatostatin-immunoreactive neurons in the rat striatum. J. Neurosci. 8 (1988) 3937-3944
122. Sherr J.D., Myers C., Avila M.T., Elliott A., Blaxton T.A., and Thaker G.K. The effects of nicotine on specific eye tracking measures in schizophrenia. Biol. Psychiatry 52 (2002) 721-728
123. Shirazi-Southall S., Rodriguez D.E., and Nomikos G.G. Effects of typical and atypical antipsychotics and receptor selective compounds on acetylcholine efflux in the hippocampus of the rat. Neuropsychopharmacology 26 (2002) 583-594
124. Singh M.M., Kay S.R., and Opler L.A. Anticholinergic-neuroleptic antagonism in terms of positive and negative symptoms of schizophrenia: Implications for psychobiological subtyping. Psychol. Med. 17 (1987) 39-48
125. Smiley J.F., Morrel F., and Mesulam M.M. Cholinergic synapses in human cerebral cortex: An ultra structural study in serial sections. Exp. Neurol 144 2 (1997) 361-368
126. Smiley J.F., Subramanian M., and Mesulam M.-M. Monoaminergic-cholinergic interactions in the primate basal forebrain. Neuroscience 93 (1999) 817-829
127. Smith R.C., Warner-Cohen J., Matute M., Butler E., Kelly E., Vaidhyanathaswamy S., and Khan A. Effects of nicotine nasal spray on cognitive function in schizophrenia. Neuropsychopharmacology 31 (2006) 637-643
128. Smythies J. Section I. The cholinergic system. Int. Rev. Neurobiol. 64 (2005) 1-122
129. Sofroniew M.V., Howe C.L., and Mobley W.C. Nerve growth factor signaling, neuroprotection, and neural repair. Annu. Rev. Neurosci. 24 (2001) 1217-1281
130. Strauss M.E., Reynolds K.S., Jayaram G., and Tune L.E. Effects of anticholinergic medication on memory in schizophrenia. Schizophr. Res. 3 (1990) 127-129
131. Stryjer R., Strous R.D., Bar F., Werber E., Shaked G., Buhiri Y., Kotler M., Weizman A., and Rabey J.M. Beneficial effect of donepezil augmentation for the management of comorbid schizophrenia and dementia. Clin. Neuropharmacol. 26 (2003) 12-17
132. Stryjer R., Strous R., Bar F., Shaked G., Shiloh R., Rozencwaig S., Grupper D., Buchman N., Kotler M., Rabey J.M., and Weizman A. Donepezil augmentation of clozapine monotherapy in schizophrenia patients: A double blind cross-over study. Hum. Psychopharmacol. 19 (2004) 343-346
133. Takahashi L.K. Prenatal stress: Consequences of glucocorticoids on hippocampal development and function. Int. J. Dev. Neurosci. 16 (1998) 199-207
134. Takahashi L.K., and Goh C.S. Glucocorticoid facilitation of cholinergic development in the rat hippocampus. Neuroscience 83 (1998) 1145-1153
135. Tanabe J., Tregellas J.R., Martin L.F., and Freedman R. Effects of nicotine on hippocampal and cingulate activity during smooth pursuit eye movement in schizophrenia. Biol. Psychiatry 59 (2006) 754-761
136. Tandon R., Shipley J.E., Greden J.F., Mann N.A., Eisner W.H., and Goodson J.A. Muscarinic cholinergic hyperactivity in schizophrenia. Relationship to positive and negative symptoms. Schizophr. Res. 4 (1991) 23-30
137. Tandon R., DeQuardo J.R., Goodson J., Mann N.A., and Greden J.F. Effect of anticholinergics on positive and negative symptoms in schizophrenia. Psychopharmacol. Bull. 28 (1992) 297-302
138. Tapper A.R., McKinney S.L., Nashmi R., Schwarz J., Deshpande P., Labarca C., Whiteaker P., Marks M.J., Collins A.C., and Lester H.A. Nicotine activation of α4 receptors: Sufficient for reward, tolerance, and sensitization. Science 306 (2004) 1029-1032
139. Thomas J.D., La Fiette M.H., Quinn V.R., and Riley E.P. Neonatal choline supplementation ameliorates the effects of prenatal alcohol exposure on a discrimination learning task in rats. Neurotoxicol. Teratol. 22 (2000) 703-711
140. Tugal O., Yazici K.M., Anil Yagcioglu A.E., and Gogus A. A double-blind, placebo controlled, cross-over trial of adjunctive donepezil for cognitive impairment in schizophrenia. Int. J. Neuropsychopharmacol. 7 (2004) 117-123
141. Tune L.E., Strauss M.E., Lew M.F., Breitlinger E., and Coyle J.T. Serum levels of anticholinergic drugs and impaired recent memory in chronic schizophrenic patients. Am. J. Psychiatry 139 (1982) 1460-1462
142. van Vulpen E.H., and van der Kooy D. Striatal cholinergic interneurons: Birthdates predict compartmental localization. Brain Res. Dev. Brain Res. 109 (1998) 51-58
143. Vizi E.S., and Kiss J.P. Neurochemistry and pharmacology of the major hippocampal transmitter systems: Synaptic and nonsynaptic interactions. Hippocampus 8 (1998) 566-607
144. Wang Z., Kai L., Day M., Ronesi J., Yin H.H., Ding J., Tkatch T., Lovinger D.M., and Surmeier D.J. Dopaminergic control of corticostriatal long-term synaptic depression in medium spiny neurons is mediated by cholinergic interneurons. Neuron 50 (2006) 443-452
145. Ward N.L., and Hagg T. BDNF is needed for postnatal maturation of basal forebrain and neostriatum cholinergic neurons in vivo. Exp. Neurol. 162 (2000) 297-310
146. Weickert C.S., Hyde T.M., Lipska B.K., Herman M.M., Weinberger D.R., and Kleinman J.E. Reduced brain-derived neurotrophic factor in prefrontal cortex of patients with schizophrenia. Mol. Psychiatry 8 (2003) 592-610
147. Weickert C.S., Ligons D.L., Romanczyk T., Ungaro G., Hyde T.M., Herman M.M., Weinberger D.R., and Kleinman J.E. Reductions in neurotrophin receptor mRNAs in the prefrontal cortex of patients with schizophrenia. Mol. Psychiatry 10 (2005) 637-650
148. Wilson C.J. Striatal D2 receptors and LTD: Yes, but not where you thought they were. Neuron 50 (2006) 347-348
149. Wolpowitz D., Mason T.B., Dietrich P., Mendelsohn M., Talmage D.A., and Role L.W. Cysteine-rich domain isoforms of the neuregulin-1 gene are required for maintenance of peripheral synapses. Neuron 25 (2000) 79-91
150. Wonnacott S., Sidhpura N., and Balfour D.J. Nicotine: From molecular mechanisms to behaviour. Curr. Opin. Pharmacol. 5 (2005) 53-59
151. Woolf N. Cholinergic systems in mammalian brain and spinal cord. Prog. Neurobiol. 37 (1991) 475-524
152. Yang X., Kuo Y., Devay P., Yu C., and Role L. A cysteine-rich isoform of neuregulin controls the level of expression of neuronal nicotinic receptor channels during synaptogenesis. Neuron 20 (1998) 255-270
153. Zemishlany Z., Aizenberg D., Weiner Z., and Weizman A. Trihexyphenidyl (Artane) abuse in schizophrenic patients. Int. Clin. Psychopharmacol. 11 (1996) 199-202
154. Zhang H., and Sulzer D. Frequency-dependent modulation of dopamine release by nicotine. Nat. Neurosci. 7 (2004) 581-582
155. Zhao Y., Marin O., Hermesz E., Powell A., Flames N., Palkovits M., Rubenstein J.L., and Westphal H. The LIM-homeobox gene Lhx8 is required for the development of many cholinergic neurons in the mouse forebrain. Proc. Natl. Acad. Sci. USA 100 (2003) 9005-9010
156. Zhou F.M., Liang Y., and Dani J.A. Endogenous nicotinic cholinergic activity regulates dopamine release in the striatum. Nat. Neurosci. 4 (2001) 1224-1229
157. Zwart R., Van Kleef R.G., and Vijverberg H.P. Physostigmine and atropine potentiate and inhibit neuronal alpha 4 beta 4 nicotinic receptors. Ann. NY Acad. Sci. 868 (1999) 636-639