Acetylcholine α7 nicotinic and dopamine D 2 receptors are targeted to many of the same postsynaptic dendrites and astrocytes in the rodent prefrontal cortex

Synapse

Volumn 65, Issue 12, 2011, Pages 1350-1367

  Duffy, Aine M ^a   Fitzgerald, Megan L ^a   Chan, June ^a   Robinson, Danielle C ^a   Milner, Teresa A ^a,c   Mackie, Kenneth ^b   Pickel, Virginia M ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b INDIANA UNIVERSITY   (United States)

^c ROCKEFELLER UNIVERSITY   (United States)

Author keywords

Electron microscopic immunolabeling; Functional hyperemia; Schizophrenia; Tripartite synapse

Indexed keywords

BUNGAROTOXIN RECEPTOR; DOPAMINE 2 RECEPTOR;

ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; ASTROCYTE; DENDRITE; ELECTRON MICROSCOPY; HUMAN; HUMAN CELL; MALE; MOUSE; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; TISSUE DISTRIBUTION;

ACETYLCHOLINE; ANIMALS; ASTROCYTES; CELL COMMUNICATION; DENDRITES; DOPAMINE; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROSCOPY, IMMUNOELECTRON; PREFRONTAL CORTEX; PRESYNAPTIC TERMINALS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, DOPAMINE D2; RECEPTORS, NICOTINIC; SYNAPTIC MEMBRANES; SYNAPTIC TRANSMISSION; VESICULAR ACETYLCHOLINE TRANSPORT PROTEINS;

EID: 80053925253     PISSN: 08874476     EISSN: 10982396     Source Type: Journal    
DOI: 10.1002/syn.20977     Document Type: Article

References (124)

1. Alves FS, Figee M, Vamelsvoort T, Veltman D, de Haan L. 2008. The revised dopamine hypothesis of schizophrenia: evidence from pharmacological MRI studies with atypical antipsychotic medication. Psychopharmacol Bull 41: 121-132.
2. Araque A, Parpura V, Sanzgiri R, Haydon P. 1998. Glutamate-dependent astrocyte modulation of synaptic transmission between cultured hippocampal neurons. Eur J Neurosci 10: 2129-2142.
3. Araque A, Parpura V, Sanzgiri RP, Haydon PG. 1999. Tripartite synapses: glia, the unacknowledged partner. Trends Neurosci 22: 208-215.
4. Arnaiz-Cot J, Gonzalez J, Sobrado M, Baldelli P, Carbone E, Gandia L, Garcia A, Hernandez-Guijo J. 2008. Allosteric modulation of alpha 7 nicotinic receptors selectively depolarizes hippocampal interneurons, enhancing spontaneous GABAergic transmission. Eur J Neurosci 27: 1097-1110.
5. Arneric S, Honig M, Milner T, Greco S, Iadecola C, Reis D. 1988. Neuronal and endothelial sites of acetylcholine synthesis and release associated with microvessels in rat cerebral cortex: ultrastructrual and neurochemical studies. Brain Res 454: 11-30.
6. Aronin N, DiFiglia M. 1992. The subcellular localization of the G-protein Gi alpha in the basal ganglia reveals its potential role in both signal transduction and vesicle trafficking. J Neurosci 12: 3435-3444.
7. Artigas F. 2010. The prefrontal cortex: a target for antipsychotic drugs. Acta Psychiatr Scand 121: 11-21.
8. Arvidsson U, Riedl M, Elde R, Meister B. 1997. Vesicular acetylcholine transporter (VAChT) protein: a novel and unique marker for cholinergic neurons in the central and peripheral nervous systems. J Comp Neurol 378: 454-467.
9. Bal A, Bachelot T, Savasta M, Manier M, Verna J, Benabid A, Feuerstein C. 1994. Evidence for dopamine D2 receptor mRNA expression by striatal astrocytes in culture: in situ hybridization and polymerase chain reaction studies. Mol Brain Res 23: 204-212.
10. Bezzi P, Carmignoto G, Pasti L, Vesce S, Rossi D, Rizzini B, Pozzan T, Volterra A. 1998. Prostaglandins stimulate calcium-dependent glutamate release in astrocytes. Nature 391: 281-285.
11. Bramanti V, Bronzi D, Tomassoni D, Li Volti G, Cannavo G, Raciti G, Napoli M, Vanella A, Campisi A, Ientile R, Avola R. 2008. Effect of choline-containing phospholipids on transglutaminase activity in primary astroglial cell cultures. Clin Exp Hypertens 30: 798-807.
12. Brana C, Aubert I, Charron G, Pellevoisin C, Bloch B. 1997. Ontogeny of the striatal neurons expressing the D2 dopamine receptor in humans: an in situ hybridization and receptor-binding study. Mol Brain Res 48: 389-400.
13. Brunelli G, Spano P, Barlati S, Guarneri B, Barbon A, Bresciani R, Pizzi M. 2005. Glutamatergic reinnervation through peripheral nerve graft dictates assembly of glutamatergic synapses at rat skeletal muscle. Proc Natl Acad Sci USA 102: 8752-8757.
14. Carr D, Sesack S. 2000. GABA-containing neurons in the rat ventral tegmental area project to the prefrontal cortex. Synapse 38: 114-123.
15. Centeno M, Henderson J, Pau K, Bethea C. 2006. Estradiol increases alpha7 nicotinic receptor in serotonergic dorsal raphe and noradrenergic locus coeruleus neurons of macaques. J Comp Neurol 497: 489-501.
16. Chan J, Aoki C, Pickel V. 1990. Optimization of differential immunogold-silver and peroxidase labeling with maintenance of ultrastructure in brain sections before plastic embedding. J Neurosci Methods 33: 113-127.
17. Choi J, Chen Y, Hamel E, Jenkins B. 2006. Brain hemodynamic changes mediated by dopamine receptors: Role of the cerebral microvasculature in dopamine-mediated neurovascular coupling. Neuroimage 30: 700-712.
18. Coggan J, Bartol T, Esquenazi E, Stiles J, Lamont S, Martone M, Berg D, Ellisman M, Sejnowski T. 2005. Evidence for ectopic neurotransmission at a neuronal synapse. Science 309: 446-451.
19. Collins A, Salminen O, Marks M, Whiteaker P, Grady S. 2009. Theroad to discovery of neuronal nicotinic cholinergic receptor subtypes. Handb Exp Pharmacol 192: 85-112.
20. Delbro D, Westerlund A, Bjorklund U, Hansson E. 2009. In inflammatory reactive astrocytes co-cultured with brain endothelial cells nicotine-evoked Ca(2+) transients are attenuated due to interleukin-1beta release and rearrangement of actin filaments. Neuroscience 159: 770-779.
21. Descarries L, Gisiger V, Steriade M. 1997. Diffuse transmission by acetylcholine in the CNS. Prog Neurobiol 53: 603-625.
22. Descarries L, Mechawar N. 2000. Ultrastructural evidence for diffuse transmission by monoamine and acetylcholine neurons of the central nervous system. Prog Brain Res 125: 27-47.
23. Dominguez Del Toro E, Juiz J, Peng X, Lindstrom J, Criado M. 1994. Immunocytochemical localization of the a7 subunit of the nicotinic acetylcholine receptor in the rat central nervous system. J Comp Neurol 349: 325-342.
24. Drake C, Milner T. 2002. Mu opioid receptors are in discrete hippocampal interneuron subpopulations. Hippocampus 12: 119-136.
25. Drenan RM, Nashmi R, Imoukhuede P, Just H, McKinney S, Lester HA. 2008. Subcellular trafficking, pentameric assembly, and subunit stoichiometry of neuronal nicotinic acetylcholine receptors containing fluorescently labeled alpha6 and beta3 subunits. Mol Pharmacol 73: 27-41.
26. Duffy A, Zhou P, Milner T, Pickel V. 2009. Spatial and intracellular relationships between the alpha7 nicotinic acetylcholine receptor and the vesicular acetylcholine transporter in the prefrontal cortex of rat and mouse. Neuroscience 161: 1091-1103.
27. Erickson J, Varoqui H, Schafer M, Modi W, Diebler M, Weihe E, Rand J, Eiden L, Bonner T, Usdin T. 1994. Functional identification of a vesicular acetylcholine transporter and its expression from a "cholinergic" gene locus. J Biol Chem 269: 21929-21932.
28. Fabian-Fine R, Skehel P, Errington M, Davies H, Sher E, Stewart M, Fine A. 2001. Ultrastructural distribution of the alpha7 nicotinic acetylcholine receptor subunit in rat hippocampus. JNeurosci 21: 7993-8003.
29. Finkbeiner S. 1993. Glial calcium. Glia 9: 83-104.
30. Fisher J, Dani J. 2000. Nicotinic receptors on hippocampal cultures can increase synaptic glutamate currents while decreasing the NMDA-receptor component. Neuropharmacology 39: 2756-2769.
31. Franklin K, Paxinos G. 1997. The mouse brain in stereotaxic coordinates. San Diego: Academic Press.
32. Free R, Hazelwood L, Cabrera D, Spalding H, Namkung Y, Rankin M, Sibley D. 2007. D1 and D2 dopamine receptor expression is regulated by direct interaction with the chaperone protein calnexin. J Biol Chem 282: 21285-21300.
33. Freedman R, Coon H, Myles-Worsley M, Orr-Urtreger A, Olincy A, Davis A, Polymeropoulos M, Holik J, Hopkins J, Hoff M, Rosenthal J, Waldo M, Reimherr F, Wender P, Yaw J, Young D, Breese C, Adams C, Patterson D, Adler L, Kruglyak L, Leonard S, Byerley W. 1997. Linkage of a neurophysiological deficit in schizophrenia to a chromosome 15 locus. Proc Natl Acad Sci USA 94: 587-592.
34. Fujii T, Masai M, Misawa H, Okuda T, Takada-Takatori Y, Moriwaki Y, Haga T, Kawashima K. 2009. Acetylcholine synthesis and release in NIH3T3 cells coexpressing the high-affinity choline transporter and choline acetyltransferase. J Neurosci Res 87: 3024-3032.
35. Fuxe K, Dahlstrom A, Jonsson G, Marcellino D, Guescini M, Dam M, Manger P, Agnati L. 2010. The discovery of central monoamine neurons gave volume transmission to the wired brain. Prog Neurobiol 90: 82-100.
36. Gabbott PL, Dickie BG, Vaid RR, Headlam AJ, Bacon SJ. 1997. Local-circuit neurones in the medial prefrontal cortex (areas 25, 32 and 24b) in the rat: morphology and quantitative distribution. J Comp Neurol 377: 465-499.
37. Garzon M, Pickel V. 2000. Dendritic and axonal targeting of the vesicular acetylcholine transporter to membranous cytoplasmic organelles in laterodorsal and pedunculopontine tegmental nuclei. J Comp Neurol 419: 32-48.
38. Garzon M, Pickel V. 2006. Subcellular distribution of M2 muscarinic receptors in relation to dopaminergic neurons of the rat ventral tegmental area. J Comp Neurol 498: 821-839.
39. Gault J, Hopkins J, Berger R, Drebing C, Logel J, Walton C, Short M, Vianzon R, Olincy A, Ross R, Adler L, Freedman R, Leonard S. 2003. Comparison of polymorphisms in the alpha7 nicotinic receptor gene and its partial duplication in schizophrenic and control subjects. Am J Med Genet B Neuropsychiatr Genet 123: 39-49.
40. Geetha T, Wooten MW. 2008. TrkA receptor endolysosomal degradation is both ubiquitin and proteasome dependent. Traffic 9: 1146-1156.
41. Gelman MS, Chang W, Thomas DY, Bergeron JJ, Prives JM. 1995. Role of the endoplasmic reticulum chaperone calnexin in subunit folding and assembly of nicotinic acetylcholine receptors. J Biol Chem 270: 15085-15092.
42. Gonzalez-Islas C, Hablitz J. 2003. Dopamine enhances EPSCs in layer II-III pyramidal neurons in rat prefrontal cortex. J Neurosci 23: 867-875.
43. Good C, Lupica C. 2009. Properties of distinct ventral tegmental area synapses activated via pedunculopontine or ventral tegmental area stimulation in vitro. J Physiol 587: 1233-1247.
44. Halassa MM, Fellin T, Haydon PG. 2007. The tripartite synapse: roles for gliotransmission in health and disease. Trends Mol Med 13: 54-63.
45. Hara Y, Yakovleva T, Bakalkin G, Pickel V. 2006. Dopamine D1 receptors have subcellular distributions conducive to interactions with prodynorphin in the rat nucleus accumbens shell. Synapse 60: 1-19.
46. Haydon PG, Carmignoto G. 2006. Astrocyte control of synaptic transmission and neurovascular coupling. Physiol Rev 86: 1009-1031.
47. Henny P, Jones B. 2008. Projections from basal forebrain to prefrontal cortex comprise cholinergic, GABAergic and glutamatergic inputs to pyramidal cells or interneurons. Eur J Neurosci 27: 654-670.
48. Iadecola C, Nedergaard M. 2007. Glial regulation of the cerebral microvasculature. Nat Neurosci 10: 1369-1376.
49. Jones I, Wonnacott S. 2004. Precise localization of alpha7 nicotinic acetylcholine receptors on glutamatergic axon terminals in the rat ventral tegmental area. J Neurosci 24: 11244-11252.
50. Kabbani N, Woll MP, Levenson R, Lindstrom JM, Changeux JP. 2007. Intracellular complexes of the beta2 subunit of the nicotinic acetylcholine receptor in brain identified by proteomics. Proc Natl Acad Sci USA 104: 20570-20575.
51. Kaplan T, Skyers P, Tabori N, Drake C, Milner T. 2004. Ultrastructural evidence for mu-opioid modulation of cholinergic pathways in rat dentate gyrus. Brain Res 1019: 28-38.
52. Kearn C, Blake-Palmer K, Daniel E, Mackie K, Glass M. 2005. Concurrent stimulation of cannabinoid CB1 and dopamine D2 receptors enhances heterodimer formation: a mechanism for receptor cross-talk? Mol Pharmacol 67: 1697-1704.
53. Keller SH, Lindstrom J, Ellisman M, Taylor P. 2001. Adjacent basic amino acid residues recognized by the COP I complex and ubiquitination govern endoplasmic reticulum to cell surface trafficking of the nicotinic acetylcholine receptor alpha-Subunit. J Biol Chem 276: 18384-18391.
54. Khan Z, Koulen P, Rubinstein M, Grandy D, Goldman-Rakic P. 2001. An astroglia-linked dopamine D2-receptor action in prefrontal cortex. Proc Natl Acad Sci USA 98: 1964-1969.
55. Kim O, Ariano M, Namkung Y, Marinec P, Kim E, Han J, Sibley D. 2008. D2 dopamine receptor expression and trafficking is regulated through direct interactions with ZIP. J Neurochem 106: 83-95.
56. Lambe E, Picciotto M, Aghajanian G. 2003. Nicotine induces glutamate release from thalamocortical terminals in prefrontal cortex. Neuropsychopharmacology 28: 216-225.
57. Lapish C, Kroener S, Durstewitz D, Lavin A, Seamans J. 2007. The ability of the mesocortical dopamine system to operate in distinct temporal modes. Psychopharmacology (Berl) 191: 609-625.
58. Laruelle M, Frankle W, Narendran R, Kegeles L, Abi-Dargham A. 2005. Mechanism of action of antipsychotic drugs: from dopamine D(2) receptor antagonism to glutamate NMDA facilitation. Clin Ther 27 Suppl A: S16-S24.
59. LeMoine C, Gaspar P. 1998. Subpopulations of cortical GABAergic interneurons differ by their expression of D1 and D2 dopamine receptor subtypes. Mol Brain Res 58: 231-236.
60. Leranth C, Pickel V, Heimer L, Zaborszky L. 1989. Electron microscopic pre-embedding double immunostaining methods. In: Neuroanatomical Tract-tracing Methods 2: Recent Progress. New York: Plenum Publishing Co. p 129-172.
61. Levin E, Rezvani A. 2007. Nicotinic interactions with antipsychotic drugs, models of schizophrenia and impacts on cognitive function. Biochem Pharmacol 74: 1182-1191.
62. Levin E, Simon B. 1998. Nicotinic acetylcholine involvement in cognitive function in animals. Psychopharmacology (Berl) 138: 217-230.
63. Levy R, Aoki C. 2002. 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.
64. Li A, Guo H, Luo X, Sheng J, Yang S, Yin Y, Zhou J. 2006. Apomorphine-induced activation of dopamine receptors modulates FGF-2 expression in astrocytic cultures and promotes survival of dopaminergic neurons. FASEB J 20: 1263-1265.
65. Livingstone P, Dickinson J, Srinivasan J, Kew J, Wonnacott S. 2010. Glutamate-dopamine crosstalk in the rat prefrontal cortex is modulated by Alpha7 nicotinic receptors and potentiated by PNU-120596. J Mol Neurosci 40: 172-176.
66. Lubin M, Erisir A, Aoki C. 1999. Ultrastructural Immunolocalization of the α7 nAChR Subunit in Guinea Pig Medial Prefrontal Cortex. Ann NY Acad Sci 868: 628-632.
67. Mandeville J, Jenkins B, Kosofsky B, Moskowitz M, Rosen B, Marota J. 2001. Regional sensitivity and coupling of BOLD and CBV changes during stimulation of rat brain. Magn Reson Med 45: 443-447.
68. Mansvelder H, van Aerde K, Couey J, Brussaard A. 2006. Nicotinic modulation of neuronal networks: from receptors to cognition. Psychopharmacol 184: 292-305.
69. Marota J, Mandeville J, Weisskoff R, Moskowitz M, Rosen B, Kosofsky B. 2000. Cocaine activation discriminates dopaminergic projections by temporal response: an fMRI study in rat. Neuroimage 11: 13-23.
70. Martina M, Bergeron R. 2008. D1 and D4 dopaminergic receptor interplay mediates coincident G protein-independent and dependent regulation of glutamate NMDA receptors in the lateral amygdala. J Neurochem 106: 2421-2435.
71. McLane K, Wu X, Lindstrom J, Conti-Tronconi B. 1992. Epitope mapping of polyclonal and monoclonal antibodies against two alpha-bungarotoxin-binding alpha subunits from neuronal nicotinic receptors. J Neuroimmunol 38: 115-128.
72. Mechawar N, Cozzari C, Descarries L. 2000. Cholinergic innervation in adult rat cerebral cortex: a quantitative immunocytochemical description. J Comp Neurol 428: 305-318.
73. Millar NS, Harkness PC. 2008. Assembly and trafficking of nicotinic acetylcholine receptors (Review). Mol Membr Biol 25: 279-292.
74. Missale C, Nash S, Robinson S, Jaber M, Caron M. 1998. Dopamine receptors: from structure to function. Physiol Rev 78: 189-225.
75. Muly EC, III, Szigeti K, Goldman-Rakic PS. 1998. D1 receptor in interneurons of macaque prefrontal cortex: distribution and subcellular localization. J Neurosci 18: 10553-10565.
76. Negyessy L, Goldman-Rakic P. 2005. Subcellular localization of the dopamine D2 receptor and coexistence with the calcium-binding protein neuronal calcium sensor-1 in the primate prefrontal cortex. J Comp Neurol 488: 464-475.
77. Oikawa H, Nakamichi N, Kambe Y, Ogura M, Yoneda Y. 2005. An increase in intracellular free calcium ions by nicotinic acetylcholine receptors in a single cultured rat cortical astrocyte. J Neurosci Res 79: 535-544.
78. Olincy A, Harris J, Johnson L, Pender V, Kongs S, Allensworth D, Ellis J, Zerbe G, Leonard S, Stevens K, Stevens J, Martin L, Adler L, Soti F, Kem W, Freedman R. 2006. Proof-of-concept trial of an alpha7 nicotinic agonist in schizophrenia. Arch Gen Psychiatry 63: 630-638.
79. Parpura V, Haydon P. 2000. Physiological astrocytic calcium levels stimulate glutamate release to modulate adjacent neurons. Proc Natl Acad Sci USA 97: 8629-8634.
80. Parri R, Crunelli V. 2003. An astrocyte bridge from synapse to blood flow. Nat Neurosci 6: 5-6.
81. Pasti L, Volterra A, Pozzan T, Carmignoto G. 1997. Intracellular calcium oscillations in astrocytes: A highly plastic, bidirectional form of communication between neurons and astrocytes in situ. J Neurosci 17: 7817-7830.
82. Patti L, Raiteri L, Grilli M, Zappettini S, Bonanno G, Marchi M. 2007. Evidence that alpha7 nicotinic receptor modulates glutamate release from mouse neocortical gliosomes. NeurochemInt 51: 1-7.
83. Paxinos G, Watson C. 1998. The rat brain in stereotaxic coordinates. San Diego: Academic Press.
84. Perea G, Araque A. 2005. Glial calcium signaling and neuron-glia communication. Cell Calcium 38: 375-382.
85. Peters A, Palay S, Webster H. 1991. The fine structure of the nervous system. New York: Oxford University Press. p 1-494.
86. Pickel V, Chan J, Kearn C, Mackie K. 2006. Targeting dopamine D2 and cannabinoid-1 (CB1) receptors in rat nucleus accumbens. J Comp Neurol 495: 299-313.
87. Pickel V, Douglas J, Chan J, Gamp P, Bunnett N. 2000. Neurokinin 1 receptor distribution in cholinergic neurons and targets of substance P terminals in the rat nucleus accumbens. J Comp Neurol 423: 500-511.
88. Pinto A, Sesack S. 2008. Ultrastructural analysis of prefrontal cortical inputs to the rat amygdala: spatial relationships to presumed dopamine axons and D1 and D2 receptors. Brain Struct Funct 213: 159-175.
89. Piper RC, Katzmann DJ. 2007. Biogenesis and function of multivesicular bodies. Annu Rev Cell Dev Biol 23: 519-547.
90. Porter J, Cauli B, Tsuzuki K, Lambolez B, Rossier J, Audinat E. 1999. Selective excitation of subtypes of neocortical interneurons by nicotinic receptors. J Neurosci 19: 5228-5235.
91. Porter LL, Rizzo E, Hornung JP. 1999. Dopamine affects parvalbumin expression during cortical development in vitro. J Neurosci 19: 8990-9003.
92. Pratt J, Winchester C, Egerton A, Cochran S, Morris B. 2008. Modelling prefrontal cortex deficits in schizophrenia: implications for treatment. Br J Pharmacol 153: S465-S470.
93. Prou D, Gu WJ, Le Crom S, Vincent JD, Salamero J, Vernier P. 2001. Intracellular retention of the two isoforms of the D(2) dopamine receptor promotes endoplasmic reticulum disruption. J Cell Sci 114: 3517-3527.
94. Reuss B, Unsicker K. 2001. Atypical neuroleptic drugs downregulate dopamine sensitivity in rat cortical and striatal astrocytes. MolCell Neurosci 18: 197-209.
95. Rezvani K, Teng Y, De Biasi M. 2010. The ubiquitin-proteasome system regulates the stability of neuronal nicotinic acetylcholine receptors. J Mol Neurosci 40: 177-184.
96. Robbins T. 2000. From arousal to cognition: the integrative position of the prefrontal cortex. Prog Brain Res 126: 469-483.
97. Roghani A, Feldman J, Kohan S, Shirzadi A, Gundersen C, Brecha N, Edwards R. 1994. Molecular cloning of a putative vesicular transporter for acetylcholine. Proc Natl Acad Sci USA 91: 10620-10624.
98. Rotaru D, Barrionuevo G, Sesack S. 2005. Mediodorsal thalamic afferents to layer III of the rat prefrontal cortex: synaptic relationships to subclasses of interneurons. J Comp Neurol 26: 220-238.
99. Sato A, Sato Y, Uchida S. 2004. Activation of the intracerebral cholinergic nerve fibers originating in the basal forebrain increases regional cerebral blood flow in the rat's cortex and hippocampus. Neurosci Lett 361: 90-93.
100. Schmued LC, Stowers CC, Scallet AC, Xu L. 2005. Fluoro-Jade C results in ultra high resolution and contrast labeling of degenerating neurons. Brain Res 1035: 24-31.
101. Schoepfer R, Conroy W, Whiting P, Gore M, Lindstrom J. 1990. Brain alpha-bungarotoxin binding protein cDNAs and MAbs reveal subtypes of this branch of the ligand-gated ion channel gene superfamily. Neuron 5: 35-48.
102. Serova L, Sabban E. 2002. Involvement of alpha 7 nicotinic acetylcholine receptors in gene expression of dopamine biosynthetic enzymes in rat brain. J Pharm Exp Ther 303: 896-903.
103. Sesack S, Hawrylak V, Melchitzky D, Lewis D. 1998. Dopamine innervation of a subclass of local circuit neurons in monkey prefrontal cortex: ultrastructural analysis of tyrosine hydroxylase and parvalbumin immunoreactive structures. Cereb Cortex 8: 614-622.
104. Severance E, Yolken R. 2008. Novel alpha7 nicotinic receptor isoforms and deficient cholinergic transcription in schizophrenia. Genes Brain Behav 7: 37-45.
105. Sharma G, Vijayaraghavan S. 2001. Nicotinic cholinergic signaling in hippocampal astrocytes involves calcium-induced calcium release from intracellular stores. Proc Natl Acad Sci USA 98: 4148-4153.
106. Simard M, Nedergaard M. 2004. The neurobiology of glia in the context of water and ion homeostasis. Neuroscience 129: 877-896.
107. Smit AB, Syed NI, Schaap D, van Minnen J, Klumperman J, Kits KS, Lodder H, van der Schors RC, van Elk R, Sorgedrager B, Brejc K, Sixma TK, Geraerts WPM. 2001. A glia-derived acetylcholine-binding protein that modulates synaptic transmission. Nature 411: 261-268.
108. Stigliani S, Zappettini S, Raiteri L, Passalacqua M, Melloni E, Venturi C, Tacchetti C, Diaspro A, Usai C, Bonanno G. 2006. Glia re-sealed particles freshly prepared from adult rat brain are competent for exocytotic release of glutamate. J Neurochem 96: 656-668.
109. Sun X, Zhao Y, Wolf M. 2005. Dopamine receptor stimulation modulates AMPA receptor synaptic insertion in prefrontal cortex neurons. J Neurosci 25: 7342-7351.
110. Svingos A, Colago E, Pickel V. 2001. Vesicular acetylcholine transporter in the rat nucleus accumbens shell: subcellular distribution and association with mu-opioid receptors. Synapse 40: 184-192.
111. Toga A, Thompson P, Mori S, Amunts K, Zilles K. 2006. Towards multimodal atlases of the human brain. Nat Rev Neurosci 7: 952-966.
112. Torrealba F, Müller C. 1999. Ultrastructure of glutamate and GABA immunoreactive axon terminals of the rat nucleus tractus solitarius, with a note on infralimbic cortex afferents. Brain Res 820: 20-30.
113. Towart L, Alves S, Znamensky V, Hayashi S, McEwen B, Milner T. 2003. Subcellular relationships between cholinergic terminals and estrogen receptor-alpha in the dorsal hippocampus. J Comp Neurol 463: 390-401.
114. Trantham-Davidson H, Kroner S, Seamans JK. 2008. Dopamine modulation of prefrontal cortex interneurons occurs independently of DARPP-32. Cereb Cortex 18: 951-958.
115. Turner T. 2004. Nicotine enhancement of dopamine release by a calcium-dependent increase in the size of the readily releasable pool of synaptic vesicles. J Neurosci 24: 11328-11336.
116. Uchida H, Graff-Guerrero A, Mulsant BH, Pollock BG, Mamo DC. 2009. Long-term stability of measuring D2 receptors in schizophrenia patients treated with antipsychotics. Schizophr Res 109: 130-133.
117. Uchida S, Kagitani F, Nakayama H, Sato A. 1997. Effect of stimulation of nicotinic cholinergic receptors on cortical cerebral blood flow and changes in the effect during aging in anesthetized rats. Neurosci Lett 228: 203-206.
118. Uteshev VV, Meyer EM, Papke RL. 2003. Regulation of neuronal function by choline and 4OH-GTS-21 through alpha 7 nicotinic receptors. J Neurophysiol 89: 1797-1806.
119. Van De Werd H, Rajkowska G, Evers P, Uylings H. 2010. Cytoarchitectonic and chemoarchitectonic characterization of the prefrontal cortical areas in the mouse. Brain Struct Funct 214: 339-353.
120. Wanamaker CP, Green WN. 2007. Endoplasmic reticulum chaperones stabilize nicotinic receptor subunits and regulate receptor assembly. J Biol Chem 282: 31113-31123.
121. Wang B, Liao W, Chang C, Wang S. 2006. Facilitation of glutamate release by nicotine involves the activation of a Ca2+/calmodulin signaling pathway in rat prefrontal cortex nerve terminals. Synapse 59: 491-501.
122. Wang H, Cuzon V, Pickel V. 2003. Postnatal development of mu-opioid receptors in the rat caudate-putamen nucleus parallels asymmetric synapse formation. Neuroscience 118: 695-708.
123. Wang Y, Goldman-Rakic P. 2004. D2 receptor regulation of synaptic burst firing in prefrontal cortical pyramidal neurons. Proc Natl Acad Sci USA 101: 5093-5098.
124. Zaborszky L, Gaykema R, Swanson D, Cullinan W. 1997. Cortical input to the basal forebrain. Neuroscience 79: 1051-1078.