Cholinergic interneuron characteristics and nicotinic properties in the striatum

Journal of Neurobiology

Volumn 53, Issue 4, 2002, Pages 590-605

  Zhou, Fu Ming ^a   Wilson, Charles J ^b   Dani, John A ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF TEXAS AT SAN ANTONIO   (United States)

Author keywords

Acetylcholine; Dopamine; Mesolimbic; Nicotine; Nucleus accumbens; Parkinson disease

Indexed keywords

DOPAMINE; DOPAMINE RECEPTOR; MUSCARINIC RECEPTOR; NICOTINIC RECEPTOR;

ACTION POTENTIAL; ARTICLE; CHOLINERGIC ACTIVITY; CHOLINERGIC NERVE CELL; CORPUS STRIATUM; DOPAMINE RELEASE; HUMAN; INTERNEURON; LEARNING; NEOSTRIATUM; NONHUMAN; NUCLEUS ACCUMBENS; OLFACTORY BULB; PRIORITY JOURNAL; SENSORIMOTOR FUNCTION;

ACETYLCHOLINE; ANIMALS; CHOLINERGIC FIBERS; CORPUS STRIATUM; DOPAMINE; HUMANS; INTERNEURONS; NEURONS, AFFERENT; RECEPTORS, DOPAMINE; RECEPTORS, NICOTINIC;

EID: 0036891570     PISSN: 00223034     EISSN: None     Source Type: Journal    
DOI: 10.1002/neu.10150     Document Type: Article

References (145)

1. Adler LE, Freedman R, Ross RG, Olincy A, Waldo MC. 1999. Elementary phenotypes in the neurobiological and genetic study of schizophrenia. Biol Psychiatry 46:8-18.
2. Aizman O, Brismar H, Uhlen P, Zettergren E, Levey AI, Forssberg H, Greengard P, Aperia A. 2000. Anatomical and physiological evidence for D1 and D2 dopamine receptor colocalization in neostriatal neurons. Nat Neurosci 3:226-230.
3. Albe-Fessard D, Rocha-Miranda C, Oswaldo-Cruz E. 1960. Activitiés évoquées dans le noyau caudé du chat en résponse á des types divers d'afférences. Electroencephalogr Clin Neurophysiol 12:649-661.
4. Albuquerque EX, Alkondon M, Pereira EF, Castro NG, Schrattenholz A, Barbosa CT, Bonfante-Cabarcas R, Aracava Y, Eisenberg HM, Maelicke A. 1997. Properties of neuronal nicotinic acetylcholine receptors: Pharmacological characterization and modulation of synaptic function. J Pharmacol Exp Ther 280:1117-1136.
5. Alcantara AA, Mrzliak L, Iakab RL, Levey AL, Hersch SM, Goldman-Rakic PS. 2001. Muscarinic m1 and m2 receptor proteins in local circuit and projection neurons of the primate striatum: Anatomical evidence for cholinergic modulation of glutamatergic prefronto-striatal pathways. J Comp Neurol 434:445-460.
6. Alkondon M, Pereira EF, Albuquerque EX. 1998. Alpha-bungarotoxin- and methyllycaconitine-sensitive nicotinic receptors mediate fast synaptic transmission in interneurons of rat hippocampal slices. Brain Res 810:257-263.
7. Anden NE, Fuxe K, Hamberger B, Hokfelt TA. 1966. Quantitative study on the nigro-neostriatal dopamine neuron system in the rat. Acta Physiol Scand 67:306-312.
8. Aosaki T, Graybiel AM, Kimura M. 1994a. Effect of the nigrostriatal dopamine system on acquired neural responses in the striatum of behaving monkeys. Science 265:412-415.
9. Aosaki T, Kimura M, Graybiel AM. 1995. Temporal and spatial characteristics of tonically active neurons of the primate's striatum. J Neurophysiol 73:1234-1252.
10. Aosaki T, Kiuchi K, Kawaguchi Y. 1998. Dopamine D1-like receptor activation excites rat striatal large aspiny neurons in vitro. J Neurosci 18:5180-5190.
11. Aosaki T, Tsubokawa H, Ishida A, Watanabe K, Graybiel AM, Kimura M. 1994b. Responses of tonically active neurons in the primate's striatum undergo systematic changes during behavioral sensorimotor conditioning. J Neurosci 14:3969-3984.
12. Bannon AW, Decker MW, Holladay MW, Curzon P, Donnelly-Roberts D, Puttfarcken PS, Bitner RS, Diaz A, Dickenson AH, Porsolt RD, Williams M, Arneric SP. 1998. Broad-spectrum, non-opioid analgesic activity by selective modulation of neuronal nicotinic acetylcholine receptors. Science 279:77-81.
13. Barbour B, Hausser M. 1997. Intersynaptic diffusion of neurotransmitter. Trends Neurosci 20:377-384.
14. Bennett BD, Callaway JC, Wilson CJ. 2000. Intrinsic membrane properties underlying spontaneous tonic firing in neostriatal cholinergic interneurons. J Neuroci 15:8493-8503.
15. Bennett BD, Wilson CJ. 1998. Synaptic regulation of action potential timing in neostriatal cholinergic interneurons. J Neurosci 18:8539-8549.
16. Bennett BD, Wilson CJ. 1999. Spontaneous activity of neostriatal cholinergic interneurons in vitro. J Neurosci 19:5586-5596.
17. 5 dopamine receptors in primate brain. J Neurosci 15:7821-7836.
18. Berke JD, Hyman SE. 2000. Addiction, dopamine, and the molecular mechanisms of memory. Neuron 25:515-532.
19. Bevan MD, Francis CM, Bolam JP. 1995. The glutamate-enriched cortical and thalamic input to neurons in the subthalamic nucleus of the rat: Convergence with GABA-positive terminals. J Comp Neurol 361:491-511.
20. Bishop GA, Chang HT, Kitai ST. 1982. Morphological and physiological properties of neostriatal neurons: An intracellular horseradish peroxidase study in the rat. Neuroscience 7:179-191.
21. Björklund A, Lindvall O. 1984. Dopamine-containing systems in the CNS. In: Björklund A, Hökfelt T, editors. Classical transmitters in the CNS, part I. Amsterdam: Elsevier, p 55-122.
22. Blazquez PM, Fujii N, Kojima J, Graybiel AM. 2002. A network representation of response probability in the striatum. Neuron 33:973-982.
23. Bolam JP, Wainer BH, Smith AD. 1984. Characterization of cholinergic neurons in the rat neostriatum. A combination of choline acetyltransferase immunocytochemistry, Golgi-impregnation and electron microscopy. Neuroscience 12:711-718.
24. Boyson SJ, McGonigle P, Molinoff PB. 1986. Quantitative autoradiographic localization of the D1 and D2 subtypes of dopamine receptors in rat brain. J Neurosci 6:3177-3188.
25. Breiter HC, Gollub RL, Weisskoff RM, Kennedy DN, Makris N, Berke JD, Goodman JM, Kantor HL, Gastfriend DR, Riorden JP, Mathew RT, Rosen BR, Hyman SE. 1997. Acute effects of cocaine on human brain activity and emotion. Neuron 19:591-611.
26. Butcher LL, Woolf NJ. 1984. Histochemical distribution of acetylcholinesterase in the central nervous system: Clues to the localization of cholinergic neurons. In: Björklund A, Hökfelt T, Kuhar MJ, editors. Classical transmitters and transmitter receptors in the CNS, part II. Amsterdam: Elsevier, p 1-50.
27. Calabresi P, Centonze D, Gubellini P, Pisani A, Bernardi G. 2000. Acetylcholine-mediated modulation of striatal function. Trends Neurosci 23:120-126.
28. Champtiaux N, Han ZY, Bessis A, Rossi FM, Zoli M, Marubio L, McIntosh JM, Changeux JP. 2002. Distribution and pharmacology of α6-containing nicotinic acetylcholine receptors analyzed with mutant mice. J Neurosci 22:1208-1217.
29. Colquhoun LM, Patrick JW. 1997. Pharmacology of neuronal nicotinic acetylcholine receptor subtypes. Adv Pharmacol 39:191-220.
30. Consolo S, Baldi G, Giorgi S, Nannini L. 1996. The cerebral cortex and parafascicular thalamic nucleus facilitate in vivo acetylcholine release in the rat striatum through distinct glutamate receptor subtypes. Eur J Neurosci 8:2702-2710.
31. Contant C, Umbriaco D, Garcia S, Watkins KC, Descarries L. 1996. Ultrastructural characterization of the acetylcholine innervation in adult rat neostriatum. Neuroscience 71:937-947.
32. Cordero-Erausquin M, Marubio LM, Klink R, Changeux JP. 2000. Nicotinic receptor function: New perspectives from knockout mice. Trends Pharmacol Sci 21:211-217.
33. Damsma G, Tham CS, Robertson GS, Fibiger HC. 1990. Dopamine D1 receptor stimulation increases striatal acetylcholine release in the rat. Eur J Pharmacol 186:335-338.
34. Dani JA. 2001. Overview of nicotinic receptors and their roles in the central nervous system. Biol Psychiatry 49: 166-174.
35. Dani JA, De Biasi M. 2001. Cellular mechanisms of nicotine addiction. Pharmacol Biochem Behav 70:439-446.
36. Dani JA, Ji D, Zhou FM. 2001. Synaptic plasticity and nicotine addiction. Neuron 31:349-352.
37. D'Aquila PS, Collu M, Gessa GL, Serra G. 2000. The role of dopamine in the mechanism of action of antidepressant drugs. Eur J Pharmacol 405:365-373.
38. DeBoer P, Abercrombie ED. 1996. Physiological release of striatal acetylcholine in vivo: Modulation by D1 and D2 dopamine receptor subtypes. J Pharmacol Exp Ther 277: 775-783.
39. De Rover M, Schoffelmeer ANM, Kits KS. 2000. Cholinergic modulation of GABAergic and glutamatergic synaptic transmission in the nucleus accumbens (NAC) shell of the rat. The 10th Neuropharmacology Conference Abstracts, p 169.
40. 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.
41. Descarries L, Gisiger V, Steriade M. 1997. Diffuse transmission by acetylcholine in the CNS. Prog Neurobiol 53:603-625.
42. Descarries L, Watkins KC, Garcia S, Bosler O, Doucet G. 1996. Dual character, asynaptic and synaptic, of the dopamine innervation in adult rat neostriatum: Aquantitative autoradiographic and immunocytochemical analysis J Comp Neurol 375:167-186.
43. Diana M, Tepper JM. 2002. Electrophysiological pharmacology of mesencephalic dopaminergic neurons. In: Di Chiara G, editor. Handbook of Experimental Pharmacology, Vol. 154/II. Dopamine in the CNS II. Berlin: Springer-Verlag, p 1-61.
44. Di Chiara G. 1999. Drug addiction as dopamine-dependent associative learning disorder. Eur J Pharmacol 375:13-30.
45. DiFiglia M, Pasik P, Pasik T. 1976. A Golgi study of neuronal types in the neostriatum of monkeys. Brain Res 114:245-256.
46. Everitt BJ, Robbins TW. 1997. Central cholinergic systems and cognition. Annu Rev Psychol 48:649-684.
47. Falkenburger BH, Barstow KL, Mintz IM. 2001. Dendrodendritic inhibition through reversal of dopamine transport. Science 293:2465-2470.
48. Frazier CJ, Buhler AV, Weiner JL, Dunwiddie TV. 1998. Synaptic potentials mediated via alpha-bungarotoxin-sensitive nicotinic acetylcholine receptors in rat hippocampal interneurons. J Neurosci 18:8228-8235.
49. Freund TF, Powell JF, Smith AD. 1984. Tyrosine hydroxylase-immunoreactive boutons in synaptic contact with identified striatonigral neurons, with particular reference to dendritic spines. Neuroscience 13:1189-1215.
50. Friedman E, Jin LQ, Cai GP, Hollon TR, Drago J, Sibley DR, Wang HY. 1997. D1-like dopaminergic activation of phosphoinositide hydrolysis is independent of D1A dopamine receptors: Evidence from D1A knockout mice. Mol Pharmacol 51:6-11.
51. Gabel LA, Nisenbaum ES. 1999. Muscarinic receptors differentially modulate the persistent potassium current in striatal spiny projection neurons. J Neurophysiol 81:1418-1423.
52. Galarraga E, Hernandez-Lopez S, Reyes A, Miranda I, Bermudez-Rattoni F, Vilchis C, Bargas J. 1999. Cholinergic modulation of neostriatal output: A functional antagonism between different types of muscarinic receptors. J Neurosci 19:3629-3638.
53. Gerfen CR, Engber TM, Mahan LC, Susel Z, Chase TN, Monsma FJ Jr, Sibley DR. 1990. D1 and D2 dopamine receptor-regulated gene expression of striatonigral and striatopallidal neurons. Science 250:1429-1432.
54. Girod R, Crabtree G, Ernstrom G, Ramirez-Latorre J, McGehee D, Turner J, Role L. 1999. Heteromeric complexes of alpha 5 and/or alpha 7 subunits. Effects of calcium and potential role in nicotine-induced presynaptic facilitation. Ann NY Acad Sci 868:578-590.
55. Gonon F. 1997. Prolonged and extrasynaptic excitatory action of dopamine mediated by D1 receptors in the rat striatum in vivo. J Neurosci 17:5972-5978.
56. Goto Y, O'Donnell P. 2001. Synchronous activity in the hippocampus and nucleus accumbens in vivo. J Neurosci 21:RC131.
57. Grace AA. 2000. Gating of information flow within the limbic system and the pathophysiology of schizophrenia. Brain Res Brain Res Rev 31:330-341.
58. Graveland GA, DiFiglia M. 1985. The frequency and distribution of medium-sized neurons with indented nuclei in the primate and rodent neostriatum. Brain Res 327:307-311.
59. Gray R, Rajan AS, Radcliffe KA, Yakehiro M, Dani JA. 1996. Hippocampal synaptic transmission enhanced by low concentrations of nicotine. Nature 383:713-716.
60. Graybiel AM, Aosaki T, Flaherty AW, Kimura M. 1994. The basal ganglia and adaptive motor control. Science 265:1826-1831.
61. Grofová I. 1979. Types of striato-nigral neurones labeled by retrograde transport of horeseradish peroxidase. Appl Neurophysiol 42:25-28.
62. Haber SN, Fudge JL, McFarland NR. 2000. Striatonigrostriatal pathways in primates form an ascending spiral from the shell to the dorsolateral striatum. J Neurosci 20:2369-2382.
63. Hebb CO. 1957. Biochemical evidence for the neural function of acetylcholine. Physiol Rev 37:196-220.
64. Hefft S, Hulo S, Bertrand D, Muller D. 1999. Synaptic transmission at nicotinic acetylcholine receptors in rat hippocampal organotypic cultures and slices. J Physiol 515:769-776.
65. Hernandez-Lopez S, Tkatch T, Perez-Garci E, Galarraga E, Bargas J, Hamm H, Surmeier DJ. 2000. D2 dopamine receptors in striatal medium spiny neurons reduce L-type Ca2+ currents and excitability via a novel PLC[beta]1-IP3-calcineurin-signaling cascade. J Neurosci 20:8987-8995.
66. Heimer L. 2000 Basal forebrain in the context of schizophrenia. Brain Res Brain Res Rev 31:205-235.
67. Hersch SM, Gutekunst CA, Rees H.D, Heilman CJ, Levey AL. 1994. Distribution of m1-m4 muscarinic receptor proteins in the rat striatum: Light and electron microscopic immunocytochemistry using subtype-specific antibodies. J Neurosci 14:3351-3363.
68. Hill JA Jr, Zoli M, Bourgeois J P, Changeux J-P. 1993. Immunocytochemical localization of a neuronal nicotinic receptor: The β2-subunit. J Neurosci 13:1551-1568.
69. 2+ currents in rat striatal neurons through parallel pathways. J Neurosci 15:458-469.
70. Imperato A, Obinu MC, Casu MA, Mascia MS, Dazzi L, Gessa GL. 1993. Evidence that neuroleptics increase striatal acetylcholine release through stimulation of dopamine D1 receptors. J Pharmacol Exp Ther 266:557-562.
71. Jones IW, Bolam JP, Wonnacott S. 2001. Presynaptic localization of the nicotinic acetylcholine receptor β2 subunit immunoreactivity in rat nigrostriatal dopaminergic neurons. J Comp Neurol 439:235-247.
72. Jones S, Sudweeks S, Yakel JL. 1999. Nicotinic receptors in the brain: Correlating physiology with function. Trends Neurosci 22:555-561.
73. Kalivas PW, Nakamura M. 1999. Neural systems for behavioral activation and reward. Curr Opin Neurobiol 9:223-227.
74. Kasa P. 1986. The cholinergic systems in brain and spinal cord. Prog Neurobiol 26:211-272.
75. Kawaguchi Y. 1993. Physiological, morphological and histochemical characterization of three classes of interneurons in rat neostriatum. J Neurosci 13:4908-4923.
76. Kebabian JW, Calne DB. 1979. Multiple receptors for dopamine. Nature 277:93-96.
77. Khan ZU, Mrzljak L, Gutierrez A, de la Calle A, Goldman-Rakic PS. 1998. Prominence of the dopamine D2 short isoform in dopaminergic pathways. Proc Natl Acad Sci USA 95:7731-7736.
78. Kimura M. 1990. Behaviorally contingent property of movement-related activity of the primate putamen. J Neurophysiol 63:1277-1296.
79. Kimura M, Kato M, Shimazaki H. 1990. Physiological properties of projection neurons in the monkey striatum to the globus pallidus. Exp Brain Res 82:672-676.
80. Kiyatkin EA, Rebec GV. 1996. Dopaminergic modulation of glutamate-induced excitations of neurons in the neostriatum and nucleus accumbens of awake, unrestrained rats. J Neurophysiol 75:142-153.
81. Klink R, de Kerchove d'Exaerde A, Zoli M, Changeux JP. 2001. Molecular and physiological diversity of nicotinic acetylcholine receptors in the midbrain dopaminergic nuclei. J Neurosci 21:1452-1463.
82. Kölliker A. 1896. Handbuch der Gewebelehre des Menchen, Bd. II. Kengleman, Leipzig.
83. Koos T, Tepper JM. 1999. Inhibitory control of neostriatal projection neurons by GABAergic interneurons. Nat Neurosci 2:467-472.
84. Koos T, Tepper JM. 2002. Dual cholinergic control of fast-spiking interneurons in the neostriatum. J Neurosci 22:529-535.
85. Kubota Y, Kawaguchi Y. 2000. Dependence of GABAergic synaptic areas on the interneuron type and target size. J Neurosci 20:375-386.
86. Lang AE, Lozano AM. 1998. Parkinson's disease. N Engl J Med 339:1130-1143.
87. Lapper SR, Bolam JP. 1992. Input from the frontal cortex and the parafascicular nucleus to cholinergic interneurons in the dorsal striatum of the rat. Neuroscience 51:533-545.
88. Leontovich TA. 1954. Fine structure of subcortical ganglia. Z Neuropat Psikh 54:168-178.
89. Levey AI, Hersch SM, Rye DB, Sunahara RK, Niznik HB, Kitt CA, Price DL, Maggio R, Brann MR, Ciliax BJ. 1993. Localization of D1 and D2 dopamine receptors in brain with subtype-specific antibodies. Proc Natl Acad Sci USA 90:8861-8865.
90. Levin ED. 1992. Nicotinic systems and cognitive function. Psychopharmacology (Berlin) 108:417-431.
91. Liang NY, Rutledge CO. 1982. Evidence for carrier-mediated efflux of dopamine from corpus striatum. Biochem Pharmacol 31:2479-2484.
92. MacIntosh FC. 1941. The distribution of acetylcholine in the peripheral and central nervous system. J Physiol 99:436-442.
93. Mansvelder HD, Keath JR, McGehee DS. 2002. Synaptic mechanisms underlie nicotine-induced excitability of brain reward areas. Neuron 33:905-919.
94. Mansvelder HD, McGehee DS. 2000. Long-term potentiation of excitatory inputs to brain reward areas by nicotine. Neuron 27:349-357.
95. Marubio LM, del Mar Arroyo-Jimenez M, Cordero-Erausquin M, Lena C, Le Novere N, de Kerchove d'Exaerde A. Huchet M, Damaj MI, Changeux JP. 1999. Reduced antinociception in mice lacking neuronal nicotinic receptor subunits. Nature 398:805-810.
96. Matsumoto N, Minamimoto T, Graybiel AM, Kimura M. 2001. Neurons in the thalamic CM-Pf complex supply striatal neurons with information about behaviorally significant sensory events. J Neurophysiol 85:960-976.
97. McGehee DS, Role LW. 1995. Physiological diversity of nicotinic acetylcholine receptors expressed by vertebrate neurons. Annu Rev Physiol 57:521-546.
98. McGehee DS, Heath MJ, Gelber S, Devay P, Role LW. 1995. Nicotine enhancement of fast excitatory synaptic transmission in CNS by presynaptic receptors. Science 269:1692-1696.
99. Mesulam, M-M. 2000. Principles of Behavioral and Cognitive Neurology. Oxford: Oxford University Press.
100. Missale C, Nash SR, Robinson SW, Jaber M, Caron MG. 1998. Dopamine receptors: From structure to function. Physiol Rev. 78:189-225.
101. Mogenson GJ, Jones DL, Yim CY. 1980. From motivation to action: Functional interface between the limbic system and the motor system. Prog Neurobiol 14:69-97.
102. Mouroux M, Feger J. 1993. Evidence that the parafascicular projection to the subthalamic nucleus is glutamatergic. Neuroreport 4:613-615.
103. Nicola SM, Surmeier J, Malenka RC. 2000. Dopaminergic modulation of neuronal excitability in the striatum and nucleus accumbens. Annu Rev Neurosci 23:185-215.
104. Oorschot DE. 1996. Total number of neurons in the neostriatal, pallidal, subthalamic, and substantia nigral nuclei of the rat basal ganglia: A stereological study using the cavalieri and optical disector methods. J Comp Neurol 366:580-599.
105. Oorschot DE. 1998. Total number of rat striatal large interneurons and thalamic parafascicular neurons: A stereological study. Int Basal Ganglia Soc Abstr 6:66.
106. Pennartz CM, Groenewegen HJ, Lopes da Silva FH. 1994. The nucleus accumbens as a complex of functionally distinct neuronal ensembles: An integration of behavioural, electrophysiological and anatomical data. Prog Neurobiol 42:719-761.
107. Phelps PE, Houser CR, Vaughn JE. 1985. Immunocytochemical localization of choline acetyltransferase within the rat neostriatum: A correlated light and electron microscopic study of cholinergic neurons and synapses. J Comp Neurol 238:286-307.
108. Picciotto MR, Zoli M, Rimondini R, Lena C, Marubio LM, Pich EM, Fuxe K, Changeux JP. 1998. Acetylcholine receptors containing the β2 subunit are involved in the reinforcing properties of nicotine. Nature 391:173-177.
109. Pickel VM, Beckley SC, Joh TH, Reis DJ. 1981. Ultrastructural immunocytochemical localization of tyrosine hydroxylase in the neostriatum. Brain Res 225:373-385.
110. Pidoplichko VI, DeBiasi M, Williams JT, Dani JA. 1997. Nicotine activates and desensitizes midbrain dopamine neurons. Nature 390:401-404.
111. Pisani A, Bonsi P, Centonze D, Calabresi P, Bernardi G. 2000. Activation of D2-like dopamine receptors reduces synaptic inputs to striatal cholinergic interneurons. J Neurosci 20:RC69.
112. Pothos EN, Davila V, Sulzer D. 1998. Presynaptic recording of quanta from midbrain dopamine neurons and modulation of the quantal size. J Neurosci 18:4106-4118.
113. Prensa L, Parent A. 2001. The nigrostriatal pathway in the rat: A single-axon study of the relationship between dorsal and ventral tier nigral neurons and the striosome/matrix striatal compartments. J Neurosci 21:7247-7260.
114. Ramon y Cajal, S. 1911. Histologie du Systeme Nerveux de L'homme et des Vertébrés. Paris: Maloine.
115. Ravel S, Legallet E, Apicella P. 1999. Tonically active neurons in the monkey striatum do not preferentially respond to appetitive stimuli. Exp Brain Res 128:531-534.
116. Ravel S, Sardo P, Legallet E, Apicella P. 2001. Reward unpredictability inside and outside of a task context as a determinant of the responses of tonically active neurons in the monkey striatum. J Neurosci 21:5730-5739.
117. Raz A, Fiengold A, Zelanskaya V, Vaadia E, Bergman, H. 1996. Neuronal synchronization of tonically active neurons in the striatum of normal and parkinsonian primates. J Neurophysiol 76:2083-2088.
118. Richfield EK, Penney JB, Young AB. 1989. Anatomical and affinity state comparisons between dopamine D1 and D2 receptors in the rat central nervous system. Neuroscience. 30:767-777.
119. Role LW, Berg DK. 1996. Nicotinic receptors in the development and modulation of CNS synapses. Neuron 16: 1077-1085.
120. Rose JE, Levin ED. 1991. Inter-relationships between conditioned and primary reinforcement in the maintenance of cigarette smoking. Br J Addict 86:605-609.
121. Sardo P, Ravel S, Legallet E, Apicella P. 2000. Influence of the predicted time of stimuli eliciting movements on responses of tonically active neurons in the monkey striatum. Eur J Neurosci 12:1801-1816.
122. Sarter M, Bruno JP. 2000. Cortical cholinergic inputs mediating arousal, attentional processing and dreaming: Differential afferent regulation of the basal forebrain by telencephalic and brainstem afferents. Neuroscience 95: 933-952.
123. Schultz W, Dayan P, Montague PR. 1997. A neural substrate of prediction and reward. Science 275:1593-1599.
124. Schwartz RD, Lehmann J, Kellar K J. 1984. Presynaptic nicotinic cholinergic receptors labeled by [3H]acetylcholine on catecholamine and serotonin axons in brain. J Neurochem 42:1495-1498.
125. Seguela P, Wadiche J, Dineley-Miller K, Dani JA, Patrick JW. 1993. Molecular cloning, functional properties, and distribution of rat brain alpha 7: A nicotinic cation channel highly permeable to calcium. J Neurosci 13:596-604.
126. Smith AD, Bolam JP. 1990. The neural network of the basal ganglia as revealed by the study of synaptic connections of identified neurones. Trends Neurosci 13:259-265.
127. Spanagel R, Weiss F. 1999. The dopamine hypothesis of reward: Past and current status. Trends Neurosci 22:521-527.
128. Thomas TM, Smith Y, Levey AI, Hersch SM. 2000. Cortical inputs to m2-immunoreactive striatal interneurons in rat and monkey. Synapse 37:252-261.
129. Uchimura N, North RA. 1990. Muscarine reduces inwardly rectifying potassium conductance in rat nucleus accumbens neurones. J Physiol 422:369-380.
130. Usiello A, Baik JH, Rouge-Pont F, Picetti R, Dierich A, LeMeur M, Piazza PV, Borrelli E. 2000. Distinct functions of the two isoforms of dopamine D2 receptors. Nature 408:199-203.
131. Wada E, Wada K, Boulter J, Deneris E, Heinemann S, Patrick J, Swanson LW. 1989. Distribution of alpha 2, alpha 3, alpha 4, and beta 2 neuronal nicotinic receptor subunit mRNAs in the central nervous system: A hybridization histochemical study in the rat. J Comp Neurol 284:314-335.
132. Waelti P, Dickenson A, Schultz W. 2002. Dopamine responses comply with basic assumptions of formal learning theory. Nature 412:43-48.
133. Watanabe K, Kimura M. 1998. Dopamine receptor-mediated mechanisms involved in the expression of learned activity of primate striatal neurons. J Neurophysiol 79: 2568-2580.
134. West AR, Grace AA. 2002. Opposite influences of endogenous dopamine D1 and D2 receptor activation on activity states and electrophysiological properties of striatal neurons: Studies combining in vivo intracellular recordings and reverse microdialysis. J Neurosci 22:294-304.
135. Wilson CJ. 1993. The generation of natural firing patterns in neostriatal neurons. Prog Brain Res 99:277-297.
136. Wilson CJ, Chang HT, Kitai ST. 1983. Origins of postsynaptic potentials evoked in spiny neostriatal projection neurons by thalamic stimulation in the rat. Exp Brain Res 51:217-226.
137. Wilson CJ, Chang, HT, Kitai ST. 1990. Firing patterns and synaptic potentials of identified giant aspiny interneurons in the rat neostriatum. J Neurosci 10:508-519.
138. Wise RA. 2000. Addiction becomes a brain disease. Neuron 26:27-33.
139. Wonnacott S. 1997. Presynaptic nicotinic ACh receptors. Trends Neurosci 20:92-98.
140. Wong AC, Shetreat ME, Clarke JO, Rayport S. 1999. D1- and D2-like dopamine receptors are co-localized on the presynaptic varicosities of striatal and nucleus accumbens neurons in vitro. Neuroscience 89:221-233.
141. Woolf NJ. 1991. Cholinergic systems in mammalian brain and spinal cord. Prog Neurobiol 37:475-524.
142. Yan Z, Flores-Hernandez J, Surmeier DJ. 2001. Coordinated expression of muscarinic receptor messenger RNAs in striatal medium spiny neurons. Neuroscience 103:1017-1024.
143. 2+ currents in rat neostriatal cholinergic interneurons through a membrane-delimited, protein-kinase-C-insensitive pathway. J Neurophysiol 77: 1003-1015.
144. 2+ currents in rat neostriatal cholinergic interneurons through a fast, membrane-delimited, G-protein pathway. J Neurosci 16:2592-2604.
145. Zhou FM, Liang Y, Dani JA. 2001. Endogenous nicotinic cholinergic activity regulates dopamine release in the striatum. Nat Neurosci 4:1224-1249.