The multilingual nature of dopamine neurons

Progress in Brain Research

Volumn 211, Issue , 2014, Pages 141-164

  Trudeau, Louis Eric ^a   Hnasko, Thomas S ^b   Wallén Mackenzie, Åsa ^c   Morales, Marisela ^d   Rayport, Steven ^e   Sulzer, David ^e,f  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UPPSALA UNIVERSITY   (Sweden)

^d NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

^e Och Spine at New York Presbyterian Hospitals   (United States)

^f NEW YORK STATE PSYCHIATRIC INSTITUTE   (United States)

Author keywords

Cotransmission; Dopamine; GABA; Glutamate; Vesicular

Indexed keywords

DOPAMINE; GLUTAMIC ACID; NEUROTRANSMITTER; VESICULAR GLUTAMATE TRANSPORTER 2; 4 AMINOBUTYRIC ACID; AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS;

ARTICLE; BRAIN; CELL SURVIVAL; CELLULAR DISTRIBUTION; CONNECTOME; CORPUS STRIATUM; DOPAMINERGIC NERVE CELL; HUMAN; NERVE CELL GROWTH; NERVE CELL PLASTICITY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SYNAPTIC TRANSMISSION; ANIMAL; METABOLISM; PHYSIOLOGY; SECRETION (PROCESS);

ANIMALS; DOPAMINERGIC NEURONS; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; HUMANS; NEUROTRANSMITTER AGENTS; SYNAPTIC TRANSMISSION;

EID: 84904619748     PISSN: 00796123     EISSN: 18757855     Source Type: Book Series    
DOI: 10.1016/B978-0-444-63425-2.00006-4     Document Type: Chapter

References (124)

1. Alsiö J., Nordenankar K., Arvidsson E., Birgner C., Mahmoudi S., Halbout B., Smith C., Fortin G.M., Olson L., Descarries L., Trudeau L.E., Kullander K., Levesque D., Wallén-Mackenzie Å. Enhanced sucrose and cocaine self-administration and cue-induced drug seeking after loss of VGLUT2 in midbrain dopamine neurons in mice. J. Neurosci. 2011, 31:12593-12603.
2. Amilhon B., Lepicard E., Renoir T., Mongeau R., Popa D., Poirel O., Miot S., Gras C., Gardier A.M., Gallego J., Hamon M., Lanfumey L., Gasnier B., Giros B., El Mestikawy S. VGLUT3 (vesicular glutamate transporter type 3) contribution to the regulation of serotonergic transmission and anxiety. J. Neurosci. 2010, 30:2198-2210.
3. Antonopoulos J., Dori I., Dinopoulos A., Chiotelli M., Parnavelas J.G. Postnatal development of the dopaminergic system of the striatum in the rat. Neuroscience 2002, 110:245-256.
4. Arbuthnott G.W., Wickens J. Space, time and dopamine. Trends Neurosci. 2007, 30:62-69.
5. Beaudet A., Descarries L. The monoamine innervation of rat cerebral cortex: synaptic and nonsynaptic axon terminals. Neuroscience 1978, 3:851-860.
6. Beckstead M.J., Grandy D.K., Wickman K., Williams J.T. Vesicular dopamine release elicits an inhibitory postsynaptic current in midbrain dopamine neurons. Neuron 2004, 42:939-946.
7. Bergquist F., Ludwig M. Dendritic transmitter release: a comparison of two model systems. J. Neuroendocrinol. 2008, 20:677-686.
8. Bergquist F., Niazi H.S., Nissbrandt H. Evidence for different exocytosis pathways in dendritic and terminal dopamine release in vivo. Brain Res. 2002, 950:245-253.
9. Bérubé-Carriere N., Riad M., Dal Bo G., Trudeau L.-E., Descarries L. Colocalisation of Dopamine and Glutamate in Axon Terminals of VTA Neurons Innervating the Nucleus Accumbens. Abstract Viewer/Itinerary Planner 2006, Society for Neuroscience, Washington, DC, Online:722.711.
10. Bérubé-Carrière N., Riad M., Dal Bo G., Lévesque D., Trudeau L.E., Descarries L. The dual dopamine-glutamate phenotype of growing mesencephalic neurons regresses in mature rat brain. J. Comp. Neurol. 2009, 517:873-891.
11. Berube-Carriere N., Guay G., Fortin G.M., Kullander K., Olson L., Wallén-Mackenzie Å., Trudeau L.E., Descarries L. Ultrastructural characterization of the mesostriatal dopamine innervation in mice, including two mouse lines of conditional VGLUT2 knockout in dopamine neurons. Eur. J. Neurosci. 2012, 35:527-538.
12. Birgner C., Nordenankar K., Lundblad M., Mendez J.A., Smith C., le Greves M., Galter D., Olson L., Fredriksson A., Trudeau L.E., Kullander K., Wallen-Mackenzie Å. VGLUT2 in dopamine neurons is required for psychostimulant-induced behavioral activation. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:389-394.
13. Bolam J.P., Pissadaki E.K. Living on the edge with too many mouths to feed: why dopamine neurons die. Mov. Disord. 2012, 27:1478-1483.
14. Boulland J.L., Qureshi T., Seal R.P., Rafiki A., Gundersen V., Bergersen L.H., Fremeau R.T.J., Edwards R.H., Storm-Mathisen J., Chaudhry F.A. Expression of the vesicular glutamate transporters during development indicates the widespread corelease of multiple neurotransmitters. J. Comp. Neurol. 2004, 480:264-280.
15. Bourque M.-J., Trudeau L.-E. GDNF enhances the synaptic efficacy of dopaminergic neurons in culture. Eur. J. Neurosci. 2000, 12:3172-3180.
16. Carlsson A. The occurrence, distribution and physiological role of catecholamines in the nervous system. Pharmacol. Rev. 1959, 11:490-493.
17. Carlsson A., Waldeck B. A fluorimetric method for the determination of dopamine (3-hydroxytyramine). Acta Physiol. Scand. 1958, 44:293-298.
18. 2+ dependence and time course of somatodendritic dopamine release: substantia nigra versus striatum. J. Neurosci. 2001, 21:7841-7847.
19. Chuhma N., Zhang H., Masson J., Zhuang X., Sulzer D., Hen R., Rayport S. Dopamine neurons mediate a fast excitatory signal via their glutamatergic synapses. J. Neurosci. 2004, 24:972-981.
20. Chuhma N., Tanaka K.F., Hen R., Rayport S. Functional connectome of the striatal medium spiny neuron. J. Neurosci. 2011, 31:1183-1192.
21. Chuhma N., Mingote S., Moore H., Rayport S. Dopamine neurons control striatal cholinergic neurons via regionally heterogeneous dopamine and glutamate signaling. Neuron 2014, 81:901-912.
22. Congar P., Bergevin A., Trudeau L.E. D2 receptors inhibit the secretory process downstream from calcium influx in dopaminergic neurons: implication of k(+) channels. J. Neurophysiol. 2002, 87:1046-1056.
23. Dal Bo G., St-Gelais F., Danik M., Williams S., Cotton M., Trudeau L.-E. Dopamine neurons in culture express VGLUT2 explaining their capacity to release glutamate at synapses in addition to dopamine. J. Neurochem. 2004, 88:1398-1405.
24. Dal Bo G., Bérubé-Carrière N., Mendez J.A., Leo D., Riad M., Descarries L., Lévesque D., Trudeau L.E. Enhanced glutamatergic phenotype of mesencephalic dopamine neurons after neonatal 6-hydroxydopamine lesion. Neuroscience 2008, 156:59-70.
25. Descarries L., Bosler O., Berthelet F., Des Rosiers M.H. Dopaminergic nerve endings visualised by high-resolution autoradiography in adult rat neostriatum. Nature 1980, 284:620-622.
26. Descarries L., Watkins K.C., Garcia S., Bosler O., Doucet G. Dual character, asynaptic and synaptic, of the dopamine innervation in adult rat neostriatum: a quantitative autoradiographic and immunocytochemical analysis. J. Comp. Neurol. 1996, 375:167-186.
27. Descarries L., Bérubé-Carrière N., Riad M., Bo G.D., Mendez J.A., Trudeau L.E. Glutamate in dopamine neurons: synaptic versus diffuse transmission. Brain Res. Rev. 2008, 58:290-302.
28. Dobi A., Margolis E.B., Wang H.L., Harvey B.K., Morales M. Glutamatergic and nonglutamatergic neurons of the ventral tegmental area establish local synaptic contacts with dopaminergic and nondopaminergic neurons. J. Neurosci. 2010, 30:218-229.
29. Edwards R.H. The neurotransmitter cycle and quantal size. Neuron 2007, 55:835-858.
30. Ekstrand M.I., Terzioglu M., Galter D., Zhu S., Hofstetter C., Lindqvist E., Thams S., Bergstrand A., Hansson F.S., Trifunovic A., Hoffer B., Cullheim S., Mohammed A.H., Olson L., Larsson N.G. Progressive parkinsonism in mice with respiratory-chain-deficient dopamine neurons. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:1325-1330.
31. El Mestikawy S., Wallén-Mackenzie Å., Fortin G.M., Descarries L., Trudeau L.E. From glutamate co-release to vesicular synergy: vesicular glutamate transporters. Nat. Rev. Neurosci. 2011, 12:204-216.
32. Everitt B.J., Meister B., Hokfelt T., Melander T., Terenius L., Rokaeus A., Theodorsson-Norheim E., Dockray G., Edwardson J., Cuello C., et al. The hypothalamic arcuate nucleus-median eminence complex: immunohistochemistry of transmitters, peptides and DARPP-32 with special reference to coexistence in dopamine neurons. Brain Res. 1986, 396:97-155.
33. Ford C.P., Gantz S.C., Phillips P.E., Williams J.T. Control of extracellular dopamine at dendrite and axon terminals. J. Neurosci. 2010, 30:6975-6983.
34. Fortin G.D., Desrosiers C.C., Yamaguchi N., Trudeau L.E. Basal somatodendritic dopamine release requires snare proteins. J. Neurochem. 2006, 96:1740-1749.
35. Fortin G.M., Bourque M.J., Mendez J.A., Leo D., Nordenankar K., Birgner C., Arvidsson E., Rymar V.V., Berube-Carriere N., Claveau A.M., Descarries L., Sadikot A.F., Wallén-Mackenzie Å., Trudeau L.E. Glutamate corelease promotes growth and survival of midbrain dopamine neurons. J. Neurosci. 2012, 32:17477-17491.
36. Fremeau R.T., Voglmaier S., Seal R.P., Edwards R.H. VGLUTs define subsets of excitatory neurons and suggest novel roles for glutamate. Trends Neurosci. 2004, 27:98-103.
37. Freund T.F., Powell J.F., Smith A.D. Tyrosine hydroxylase-immunoreactive boutons in synaptic contact with identified striatonigral neurons, with particular reference to dendritic spines. Neuroscience 1984, 13:1189-1215.
38. Fujita M., Shimada S., Nishimura T., Uhl G.R., Tohyama M. Ontogeny of dopamine transporter mRNA expression in the rat brain. Brain Res. Mol. Brain Res. 1993, 19:222-226.
39. Gantz S.C., Bunzow J.R., Williams J.T. Spontaneous inhibitory synaptic currents mediated by a G protein-coupled receptor. Neuron 2013, 78:807-812.
40. Gaugler M.N., Genc O., Bobela W., Mohanna S., Ardah M.T., El-Agnaf O.M., Cantoni M., Bensadoun J.C., Schneggenburger R., Knott G.W., Aebischer P., Schneider B.L. Nigrostriatal overabundance of alpha-synuclein leads to decreased vesicle density and deficits in dopamine release that correlate with reduced motor activity. Acta Neuropathol. 2012, 123:653-669.
41. Gauthier J., Parent M., Lévesque M., Parent A. The axonal arborization of single nigrostriatal neurons in rats. Brain Res. 1999, 834:228-232.
42. Geffen L.B., Jessell T.M., Cuello A.C., Iversen L.L. Release of dopamine from dendrites in rat substantia nigra. Nature 1976, 260:258-260.
43. German D.C., Schlusselberg D.S., Woodward D.J. Three-dimensional computer reconstruction of midbrain dopaminergic neuronal populations: from mouse to man. J. Neural Transm. 1983, 57:243-254.
44. Gorelova N., Mulholland P.J., Chandler L.J., Seamans J.K. The glutamatergic component of the mesocortical pathway emanating from different subregions of the ventral midbrain. Cereb. Cortex 2012, 22:327-336.
45. Gras C., Amilhon B., Lepicard E.M., Poirel O., Vinatier J., Herbin M., Dumas S., Tzavara E.T., Wade M.R., Nomikos G.G., Hanoun N., Saurini F., Kemel M.L., Gasnier B., Giros B., El Mestikawy S. The vesicular glutamate transporter VGLUT3 synergizes striatal acetylcholine tone. Nat. Neurosci. 2008, 11:292-300.
46. Groves P.M., Wilson C.J., Young S.J., Rebec G.V. Self-inhibition by dopaminergic neurons. Science 1975, 190:522-528.
47. Groves P.M., Linder J.C., Young S.J. 5-hydroxydopamine-labeled dopaminergic axons: three-dimensional reconstructions of axons, synapses and postsynaptic targets in rat neostriatum. Neuroscience 1994, 58:593-604.
48. Harfstrand A. Intraventricular administration of neuropeptide Y (NPY) induces hypotension, bradycardia and bradypnoea in the awake unrestrained male rat. Counteraction by NPY-induced feeding behaviour. Acta Physiol. Scand. 1986, 128:121-123.
49. Hattori T., Takada M., Moriizumi T., Van der Kooy D. Single dopaminergic nigrostriatal neurons form two chemically distinct synaptic types: possible transmitter segregation within neurons. J. Comp. Neurol. 1991, 309:391-401.
50. Hery F., Ternaux J.P. Regulation of release processes in central serotoninergic neurons. J. Physiol. 1981, 77:287-301.
51. Hirasawa H., Betensky R.A., Raviola E. Corelease of dopamine and GABA by a retinal dopaminergic neuron. J. Neurosci. 2012, 32:13281-13291.
52. Hnasko T.S., Edwards R.H. Neurotransmitter corelease: mechanism and physiological role. Annu. Rev. Physiol. 2012, 74:225-243.
53. Hnasko T.S., Chuhma N., Zhang H., Goh G.Y., Sulzer D., Palmiter R.D., Rayport S., Edwards R.H. Vesicular glutamate transport promotes dopamine storage and glutamate corelease in vivo. Neuron 2010, 65:643-656.
54. Hnasko T.S., Hjelmstad G.O., Fields H.L., Edwards R.H. Ventral tegmental area glutamate neurons: electrophysiological properties and projections. J. Neurosci. 2012, 32:15076-15085.
55. Hökfelt T., Lundberg J.M., Schultzberg M., Johansson O., Skirboll L., Anggard A., Fredholm B., Hamberger B., Pernow B., Rehfeld J., Goldstein M. Cellular localization of peptides in neural structures. Proc. R. Soc. Lond. B Biol. Sci. 1980, 210:63-77.
56. Hökfelt T., Everitt B.J., Theodorsson-Norheim E., Goldstein M. Occurrence of neurotensinlike immunoreactivity in subpopulations of hypothalamic, mesencephalic, and medullary catecholamine neurons. J. Comp. Neurol. 1984, 222:543-559.
57. Hökfelt T., Johansson O., Goldstein M. Chemical anatomy of the brain. Science (New York, NY) 1984, 225:1326-1334.
58. Ishikawa M., Otaka M., Neumann P.A., Wang Z., Cook J.M., Schlüter O.M., Dong Y., Huang Y.H. Exposure to cocaine regulates inhibitory synaptic transmission from the ventral tegmental area to the nucleus accumbens. J. Physiol. Lond. 2013, 591:4827-4841.
59. Johnson M.D. Synaptic glutamate release by postnatal rat serotonergic neurons in microculture. Neuron 1994, 12:433-442.
60. Johnson R.G., Carty S.E., Scarpa A. Proton: substrate stoichiometries during active transport of biogenic amines in chromaffin ghosts. J. Biol. Chem. 1981, 256:5773-5780.
61. Joyce M.P., Rayport S. Mesoaccumbens dopamine neuron synapses reconstructed in vitro are glutamatergic. Neuroscience 2000, 99:445-456.
62. Kalivas P.W., Deutch A.Y., Maggio J.E., Mantyh P.W., Roth R.H. Substance K and substance P in the ventral tegmental area. Neurosci. Lett. 1985, 57:241-246.
63. Kaneko T., Akiyama H., Nagatsu I., Mizuno N. Immunohistochemical demonstration of glutaminase in catecholaminergic and serotoninergic neurons of rat brain. Brain Res. 1990, 507:151-154.
64. Kawano M., Kawasaki A., Sakata-Haga H., Fukui Y., Kawano H., Nogami H., Hisano S. Particular subpopulations of midbrain and hypothalamic dopamine neurons express vesicular glutamate transporter 2 in the rat brain. J. Comp. Neurol. 2006, 498:581-592.
65. +-linked dopamine transport in chromaffin granule ghosts. Biochemistry 1981, 20:6625-6629.
66. Koos T., Tecuapetla F., Tepper J.M. Glutamatergic signaling by midbrain dopaminergic neurons: recent insights from optogenetic, molecular and behavioral studies. Curr. Opin. Neurobiol. 2011, 21:393-401.
67. Korf J., Zieleman M., Westerink B.H. Dopamine release in substantia nigra?. Nature 1976, 260:257-258.
68. Lapish C.C., Kroener S., Durstewitz D., Lavin A., Seamans J.K. The ability of the mesocortical dopamine system to operate in distinct temporal modes. Psychopharmacology (Berl) 2007, 191:609-625.
69. Lavin A., Nogueira L., Lapish C.C., Wightman R.M., Phillips P.E., Seamans J.K. Mesocortical dopamine neurons operate in distinct temporal domains using multimodal signaling. J. Neurosci. 2005, 25:5013-5023.
70. Le W.D., Bostwick J.R., Appel S.H. Use of [3H]-GBR12935 to measure dopaminergic nerve terminal growth into the developing rat striatum. Brain Res. Dev. Brain Res. 1992, 67:375-377.
71. Li X., Qi J., Yamaguchi T., Wang H.L., Morales M. Heterogeneous composition of dopamine neurons of the rat A10 region: molecular evidence for diverse signaling properties. Brain Struct. Funct. 2013, 218:1159-1176.
72. Liu S., Plachez C., Shao Z., Puche A., Shipley M.T. Olfactory bulb short axon cell release of GABA and dopamine produces a temporally biphasic inhibition-excitation response in external tufted cells. J. Neurosci. 2013, 33:2916-2926.
73. Lynd-Balta E., Haber S.N. The organization of midbrain projections to the ventral striatum in the primate. Neuroscience 1994, 59:609-623.
74. Lynd-Balta E., Haber S.N. The organization of midbrain projections to the striatum in the primate: sensorimotor-related striatum versus ventral striatum. Neuroscience 1994, 59:625-640.
75. Marquez J., Tosina M., de la Rosa V., Segura J.A., Alonso F.J., Mates J.M., Campos-Sandoval J.A. New insights into brain glutaminases: beyond their role on glutamatergic transmission. Neurochem. Int. 2009, 55:64-70.
76. Matsuda W., Furuta T., Nakamura K.C., Hioki H., Fujiyama F., Arai R., Kaneko T. Single nigrostriatal dopaminergic neurons form widely spread and highly dense axonal arborizations in the neostriatum. J. Neurosci. 2009, 29:444-453.
77. Maycox P.R., Deckwerth T., Hell J.W., Jahn R. Glutamate uptake by brain synaptic vesicles. Energy dependence of transport and functional reconstitution in proteoliposomes. J. Biol. Chem. 1988, 263:15423-15428.
78. Mendez J.A., Bourque M.J., Dal Bo G., Bourdeau M.L., Danik M., Williams S., Lacaille J.C., Trudeau L.E. Developmental and target-dependent regulation of vesicular glutamate transporter expression by dopamine neurons. J. Neurosci. 2008, 28:6309-6318.
79. Mendez J.A., Bourque M.J., Fasano C., Kortleven C., Trudeau L.E. Somatodendritic dopamine release requires synaptotagmin 4 and 7 and the participation of voltage-gated calcium channels. J. Biol. Chem. 2011, 286:23928-23937.
80. Montagu K.A. Catechol compounds in rat tissues and in brains of different animals. Nature 1957, 180:244-245.
81. Moss J., Ungless M.A., Bolam J.P. Dopaminergic axons in different divisions of the adult rat striatal complex do not express vesicular glutamate transporters. Eur. J. Neurosci. 2011, 33:1205-1211.
82. Murakami S., Okamura H., Pelletier G., Ibata Y. Differential colocalization of neuropeptide Y- and methionine-enkephalin-Arg6-Gly7-Leu8-like immunoreactivity in catecholaminergic neurons in the rat brain stem. J. Comp. Neurol. 1989, 281:532-544.
83. Nair-Roberts R.G., Chatelain-Badie S.D., Benson E., White-Cooper H., Bolam J.P., Ungless M.A. Stereological estimates of dopaminergic, GABAergic and glutamatergic neurons in the ventral tegmental area, substantia nigra and retrorubral field in the rat. Neuroscience 2008, 152:1024-1031.
84. Nieoullon A., Cheramy A., Glowinski J. Release of dopamine in vivo from cat substantia nigra. Nature 1977, 266:375-377.
85. Nirenberg M.J., Vaughan R.A., Uhl G.R., Kuhar M.J., Pickel V.M. The dopamine transporter is localized to dendritic and axonal plasma membranes of nigrostriatal dopaminergic neurons. J. Neurosci. 1996, 15:436-447.
86. Omiatek D.M., Bressler A.J., Cans A.S., Andrews A.M., Heien M.L., Ewing A.G. The real catecholamine content of secretory vesicles in the CNS revealed by electrochemical cytometry. Sci. Rep. 2013, 3:1447.
87. Omote H., Miyaji T., Juge N., Moriyama Y. Vesicular neurotransmitter transporter: bioenergetics and regulation of glutamate transport. Biochemistry 2011, 50:5558-5565.
88. Oorschot D.E. 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. 1996, 366:580-599.
89. Ottersen O.P., Storm-Mathisen J. Glutamate- and GABA-containing neurons in the mouse and rat brain, as demonstrated with a new immunocytochemical technique. J. Comp. Neurol. 1984, 229:374-392.
90. Pereira D.B., Sulzer D. Mechanisms of dopamine quantal size regulation. Front. Biosci. 2012, 17:2740-2767.
91. Perrone-Capano C., Tino A., di Porzio U. Target cells modulate dopamine transporter gene expression during brain development. Neuroreport 1994, 5:1145-1148.
92. Pickel V.M., Beckley S.C., Joh T.H., Reis D.J. Ultrastructural immunocytochemical localization of tyrosine hydroxylase in the neostriatum. Brain Res. 1981, 225:373-385.
93. Prensa L., Parent A. 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. 2001, 21:7247-7260.
94. Prensa L., Gimenez-Amaya J.M., Parent A., Bernacer J., Cebrian C. The nigrostriatal pathway: axonal collateralization and compartmental specificity. J. Neural Transm. Suppl. 2009, 49-58.
95. Rodriguez P.C., Pereira D.B., Borgkvist A., Wong M.Y., Barnard C., Sonders M.S., Zhang H., Sames D., Sulzer D. Fluorescent dopamine tracer resolves individual dopaminergic synapses and their activity in the brain. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:870-875.
96. Schafer M.K., Varoqui H., Defamie N., Weihe E., Erickson J.D. Molecular cloning and functional identification of mouse vesicular glutamate transporter 3 and its expression in subsets of novel excitatory neurons. J. Biol. Chem. 2002, 277:50734-50748.
97. Schimchowitsch S., Vuillez P., Tappaz M.L., Klein M.J., Stoeckel M.E. Systematic presence of GABA-immunoreactivity in the tubero-infundibular and tubero-hypophyseal dopaminergic axonal systems: an ultrastructural immunogold study on several mammals. Exp. Brain Res. 1991, 83:575-586.
98. Schmitz Y., Schmauss C., Sulzer D. Altered dopamine release and uptake kinetics in mice lacking D2 receptors. J. Neurosci. 2002, 22:8002-8009.
99. Schmitz Y., Luccarelli J., Kim M., Wang M., Sulzer D. Glutamate controls growth rate and branching of dopaminergic axons. J. Neurosci. 2009, 29:11973-11981.
100. Schmitz Y., Castagna C., Mrejeru A., Lizardi-Ortiz J.E., Klein Z., Lindsley C.W., Sulzer D. Glycine transporter-1 inhibition promotes striatal axon sprouting via NMDA receptors in dopamine neurons. J. Neurosci. 2013, 33:16778-16789.
101. Schultz W. Updating dopamine reward signals. Curr. Opin. Neurobiol. 2013, 23:229-238.
102. Schultz W., Dayan P., Montague P.R. A neural substrate of prediction and reward. Science 1997, 275:1593-1599.
103. Seamans J.K., Yang C.R. The principal features and mechanisms of dopamine modulation in the prefrontal cortex. Prog. Neurobiol. 2004, 74:1-58.
104. Seroogy K., Ceccatelli S., Schalling M., Hokfelt T., Frey P., Walsh J., Dockray G., Brown J., Buchan A., Goldstein M. A subpopulation of dopaminergic neurons in rat ventral mesencephalon contains both neurotensin and cholecystokinin. Brain Res. 1988, 455:88-98.
105. Smith Y., Bennett B.D., Bolam J.P., Parent A., Sadikot A.F. Synaptic relationships between dopaminergic afferents and cortical or thalamic input in the sensorimotor territory of the striatum in monkey. J. Comp. Neurol. 1994, 344:1-19.
106. Staal R.G., Mosharov E.V., Sulzer D. Dopamine neurons release transmitter via a flickering fusion pore. Nat. Neurosci. 2004, 7:341-346.
107. Stamatakis A.M., Jennings J.H., Ung R.L., Blair G.A., Weinberg R.J., Neve R.L., Boyce F., Mattis J., Ramakrishnan C., Deisseroth K., Stuber G.D. A unique population of ventral tegmental area neurons inhibits the lateral habenula to promote reward. Neuron 2013, 80:1039-1053.
108. Stornetta R.L., Sevigny C.P., Schreihofer A.M., Rosin D.L., Guyenet P.G. Vesicular glutamate transporter DNPI/VGLUT2 is expressed by both C1 adrenergic and nonaminergic presympathetic vasomotor neurons of the rat medulla. J. Comp. Neurol. 2002, 444:207-220.
109. Stuber G.D., Hnasko T.S., Britt J.P., Edwards R.H., Bonci A. Dopaminergic terminals in the nucleus accumbens but not the dorsal striatum corelease glutamate. J. Neurosci. 2010, 30:8229-8233.
110. Studler J.M., Kitabgi P., Tramu G., Herve D., Glowinski J., Tassin J.P. Extensive co-localization of neurotensin with dopamine in rat meso-cortico-frontal dopaminergic neurons. Neuropeptides 1988, 11:95-100.
111. Sulzer D., Pothos E.N. Regulation of quantal size by presynaptic mechanisms. Rev. Neurosci. 2000, 11:159-212.
112. Sulzer D., Joyce M.P., Lin L., Geldwert D., Haber S.N., Hattori T., Rayport S. Dopamine neurons make glutamatergic synapses in vitro. J. Neurosci. 1998, 18:4588-4602.
113. Swanson L.W. The projections of the ventral tegmental area and adjacent regions: a combined fluorescent retrograde tracer and immunofluorescence study in the rat. Brain Res. Bull. 1982, 9:321-353.
114. Tabb J.S., Kish P.E., Van Dyke R., Ueda T. Glutamate transport into synaptic vesicles. Roles of membrane potential, pH gradient, and intravesicular pH. J. Biol. Chem. 1992, 267:15412-15418.
115. Tecuapetla F., Patel J.C., Xenias H., English D., Tadros I., Shah F., Berlin J., Deisseroth K., Rice M.E., Tepper J.M., Koos T. Glutamatergic signaling by mesolimbic dopamine neurons in the nucleus accumbens. J. Neurosci. 2010, 30:7105-7110.
116. Tritsch N.X., Ding J.B., Sabatini B.L. Dopaminergic neurons inhibit striatal output through non-canonical release of GABA. Nature 2012, 490:262-266.
117. Trudeau L.-E., Gutierrez R. On cotransmission and neurotransmitter phenotype plasticity. Mol. Interv. 2007, 7(3):138-146.
118. Wallén-Mackenzie Å., Wootz H., Englund H. Genetic inactivation of the vesicular glutamate transporter 2 (VGLUT2) in the mouse: what have we learnt about functional glutamatergic neurotransmission?. Ups. J. Med. Sci. 2010, 115:11-20.
119. Wilson C.J., Chang H.T., Kitai S.T. Origins of postsynaptic potentials evoked in identified rat neostriatal neurons by stimulation in substantia nigra. Exp. Brain Res. 1982, 45:157-167.
120. Witkovsky P., Patel J.C., Lee C.R., Rice M.E. Immunocytochemical identification of proteins involved in dopamine release from the somatodendritic compartment of nigral dopaminergic neurons. Neuroscience 2009, 164:488-496.
121. Yamaguchi T., Sheen W., Morales M. Glutamatergic neurons are present in the rat ventral tegmental area. Eur. J. Neurosci. 2007, 25:106-118.
122. Yamaguchi T., Wang H.L., Li X., Ng T.H., Morales M. Mesocorticolimbic glutamatergic pathway. J. Neurosci. 2011, 31:8476-8490.
123. Yamaguchi T., Wang H.L., Morales M. Glutamate neurons in the substantia nigra compacta and retrorubral field. Eur. J. Neurosci. 2013, 38:3602-3610.
124. Zhuang X., Masson J., Gingrich J.A., Rayport S., Hen R. Targeted gene expression in dopamine and serotonin neurons of the mouse brain. J. Neurosci. Methods 2005, 143:27-32.