Glutamatergic and dopaminergic neurons in the mouse ventral tegmental area

European Journal of Neuroscience

Volumn 41, Issue 6, 2015, Pages 760-772

  Yamaguchi, Tsuyoshi ^a,b   Qi, Jia ^a   Wang, Hui Ling ^a   Zhang, Shiliang ^a   Morales, Marisela ^a  

^a NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

^b DOKKYO MEDICAL UNIVERSITY   (Japan)

Author keywords

Interpeduncular nucleus; Lateral habenula; Optogenetics reward; Ventral tegmental area; VGluT2

Indexed keywords

CRE RECOMBINASE; MESSENGER RNA; TYROSINE 3 MONOOXYGENASE; VESICULAR GLUTAMATE TRANSPORTER 2; GLUTAMIC ACID DERIVATIVE; SLC17A6 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL LEVEL; CELL POPULATION; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; GLUTAMATERGIC NEURON; HABENULA; IMMUNOFLUORESCENCE; MALE; MOUSE; NERVE CELL; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; RAT; VENTRAL TEGMENTUM; ANIMAL; C57BL MOUSE; METABOLISM; SPECIES DIFFERENCE; SPRAGUE DAWLEY RAT;

ANIMALS; DOPAMINERGIC NEURONS; GLUTAMATES; MALE; MICE; MICE, INBRED C57BL; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; SPECIES SPECIFICITY; TYROSINE 3-MONOOXYGENASE; VENTRAL TEGMENTAL AREA; VESICULAR GLUTAMATE TRANSPORT PROTEIN 2;

EID: 84925203366     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12818     Document Type: Article

References (43)

1. Adrover, M.F., Shin, J.H. & Alvarez, V.A. (2014) Glutamate and dopamine transmission from midbrain dopamine neurons share similar release properties but are differentially affected by cocaine. J. Neurosci., 34, 3183-3192.
2. Alsio, 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. & Wallen-Mackenzie, A. (2011) Enhanced sucrose and cocaine self-administration and cue-induced drug seeking after loss of VGLUT2 in midbrain dopamine neurons in mice. J. Neurosci., 31, 12593-12603.
3. 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, A. (2010) VGLUT2 in dopamine neurons is required for psychostimulant-induced behavioral activation. Proc. Natl. Acad. Sci. USA, 107, 389-394.
4. Borgius, L., Restrepo, C.E., Leao, R.N., Saleh, N. & Kiehn, O. (2010) A transgenic mouse line for molecular genetic analysis of excitatory glutamatergic neurons. Mol. Cell. Neurosci., 45, 245-257.
5. Chuhma, N., Mingote, S., Moore, H. & Rayport, S. (2014) Dopamine neurons control striatal cholinergic neurons via regionally heterogeneous dopamine and glutamate signaling. Neuron, 81, 901-912.
6. 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., Wallen-Mackenzie, A. & Trudeau, L.E. (2012) Glutamate corelease promotes growth and survival of midbrain dopamine neurons. J. Neurosci., 32, 17477-17491.
7. Geisler, S., Derst, C., Veh, R.W. & Zahm, D.S. (2007) Glutamatergic afferents of the ventral tegmental area in the rat. J. Neurosci., 27, 5730-5743.
8. German, D.C. & Manaye, K.F. (1993) Midbrain dopaminergic neurons (nuclei A8, A9, and A10): three-dimensional reconstruction in the rat. J. Comp. Neurol., 331, 297-309.
9. Halliday, G.M. & Tork, I. (1986) Comparative anatomy of the ventromedial mesencephalic tegmentum in the rat, cat, monkey and human. J. Comp. Neurol., 252, 423-445.
10. Hnasko, T.S., Chuhma, N., Zhang, H., Goh, G.Y., Sulzer, D., Palmiter, R.D., Rayport, S. & Edwards, R.H. (2010) Vesicular glutamate transport promotes dopamine storage and glutamate corelease in vivo. Neuron, 65, 643-656.
11. Hnasko, T.S., Hjelmstad, G.O., Fields, H.L. & Edwards, R.H. (2012) Ventral tegmental area glutamate neurons: electrophysiological properties and projections. J. Neurosci., 32, 15076-15085.
12. Hur, E.E. & Zaborszky, L. (2005) Vglut2 afferents to the medial prefrontal and primary somatosensory cortices: a combined retrograde tracing in situ hybridization study [corrected]. J. Comp. Neurol., 483, 351-373.
13. Ikemoto, S. (2007) Dopamine reward circuitry: two projection systems from the ventral midbrain to the nucleus accumbens-olfactory tubercle complex. Brain Res. Rev., 56, 27-78.
14. Ilango, A., Kesner, A.J., Broker, C.J., Wang, D.V. & Ikemoto, S. (2014) Phasic excitation of ventral tegmental dopamine neurons potentiates the initiation of conditioned approach behavior: parametric and reinforcement-schedule analyses. Front. Behav. Neurosci., 8, 155.
15. Kawano, M., Kawasaki, A., Sakata-Haga, H., Fukui, Y., Kawano, H., Nogami, H. & Hisano, S. (2006) Particular subpopulations of midbrain and hypothalamic dopamine neurons express vesicular glutamate transporter 2 in the rat brain. J. Comp. Neurol., 498, 581-592.
16. Lammel, S., Lim, B.K. & Malenka, R.C. (2014) Reward and aversion in a heterogeneous midbrain dopamine system. Neuropharmacology, 76, 351-359.
17. Li, X., Qi, J., Yamaguchi, T., Wang, H.L. & Morales, M. (2013) Heterogeneous composition of dopamine neurons of the rat A10 region: molecular evidence for diverse signaling properties. Brain Struct. Funct., 218, 1159-1176.
18. Margolis, E.B., Lock, H., Hjelmstad, G.O. & Fields, H.L. (2006) The ventral tegmental area revisited: is there an electrophysiological marker for dopaminergic neurons? J. Physiol., 577, 907-924.
19. Morales, M. & Pickel, V.M. (2012) Insights to drug addiction derived from ultrastructural views of the mesocorticolimbic system. Ann. NY Acad. Sci., 1248, 71-88.
20. Morales, M. & Root, D.H. (2014) Glutamate neurons within the midbrain dopamine regions. Neuroscience, 282C, 60-68.
21. Morales, M. & Wang, S.D. (2002) Differential composition of 5-hydroxytryptamine3 receptors synthesized in the rat CNS and peripheral nervous system. J. Neurosci., 22, 6732-6741.
22. Nair-Roberts, R.G., Chatelain-Badie, S.D., Benson, E., White-Cooper, H., Bolam, J.P. & Ungless, M.A. (2008) Stereological estimates of dopaminergic, GABAergic and glutamatergic neurons in the ventral tegmental area, substantia nigra and retrorubral field in the rat. Neuroscience, 152, 1024-1031.
23. Nordenankar, K., Smith-Anttila, C.J., Schweizer, N., Viereckel, T., Birgner, C., Mejia-Toiber, J., Morales, M., Leao, R.N. & Wallen-Mackenzie, A. (2014) Increased hippocampal excitability and impaired spatial memory function in mice lacking VGLUT2 selectively in neurons defined by tyrosine hydroxylase promoter activity. Brain Struct. Funct., doi:10.1007/s00429-014-0778-9. [Epub ahead of print].
24. Paxinos, G. & Franklin, K.B.J. (2001) The Mouse Brain in Stereotaxic Coordinates. Academic Press, New York.
25. Paxinos, G. & Watson, C. (2007) The Rat Brain in Stereotaxic Coordinates. Elsevier, Amsterdam.
26. Phillipson, O.T. (1979a) The cytoarchitecture of the interfascicular nucleus and ventral tegmental area of Tsai in the rat. J. Comp. Neurol., 187, 85-98.
27. Phillipson, O.T. (1979b) A Golgi study of the ventral tegmental area of Tsai and interfascicular nucleus in the rat. J. Comp. Neurol., 187, 99-115.
28. Root, D.H., Mejias-Aponte, C.A., Qi, J. & Morales, M. (2014a) Role of glutamatergic projections from ventral tegmental area to lateral habenula in aversive conditioning. J. Neurosci., 34, 13906-13910.
29. Root, D.H., Mejias-Aponte, C.A., Zhang, S., Wang, H.L., Hoffman, A.F., Lupica, C.R. & Morales, M. (2014b) Single rodent mesohabenular axons release glutamate and GABA. Nat. Neurosci., 17, 1543-1551.
30. Sesack, S.R. & Grace, A.A. (2010) Cortico-Basal Ganglia reward network: microcircuitry. Neuropsychopharmacology, 35, 27-47.
31. Sesack, S.R., Carr, D.B., Omelchenko, N. & Pinto, A. (2003) Anatomical substrates for glutamate-dopamine interactions: evidence for specificity of connections and extrasynaptic actions. Ann. NY Acad. Sci., 1003, 36-52.
32. 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. (2013) A unique population of ventral tegmental area neurons inhibits the lateral habenula to promote reward. Neuron, 80, 1039-1053.
33. Stuber, G.D., Hnasko, T.S., Britt, J.P., Edwards, R.H. & Bonci, A. (2010) Dopaminergic terminals in the nucleus accumbens but not the dorsal striatum corelease glutamate. J. Neurosci., 30, 8229-8233.
34. Swanson, L.W. (1982) The projections of the ventral tegmental area and adjacent regions: a combined fluorescent retrograde tracer and immunofluorescence study in the rat. Brain Res. Bull., 9, 321-353.
35. Tagliaferro, P. & Morales, M. (2008) Synapses between corticotropin-releasing factor-containing axon terminals and dopaminergic neurons in the ventral tegmental area are predominantly glutamatergic. J. Comp. Neurol., 506, 616-626.
36. Tan, K.R., Yvon, C., Turiault, M., Mirzabekov, J.J., Doehner, J., Labouebe, G., Deisseroth, K., Tye, K.M. & Luscher, C. (2012) GABA neurons of the VTA drive conditioned place aversion. Neuron, 73, 1173-1183.
37. Taylor, S.R., Badurek, S., Dileone, R.J., Nashmi, R., Minichiello, L. & Picciotto, M.R. (2014) GABAergic and glutamatergic efferents of the mouse ventral tegmental area. J. Comp. Neurol., 552, 3308-3334.
38. 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. (2010) Glutamatergic signaling by mesolimbic dopamine neurons in the nucleus accumbens. J. Neurosci., 30, 7105-7110.
39. Wang, H.L. & Morales, M. (2008) Corticotropin-releasing factor binding protein within the ventral tegmental area is expressed in a subset of dopaminergic neurons. J. Comp. Neurol., 509, 302-318.
40. Yamaguchi, T., Sheen, W. & Morales, M. (2007) Glutamatergic neurons are present in the rat ventral tegmental area. Eur. J. Neurosci., 25, 106-118.
41. Yamaguchi, T., Wang, H.L., Li, X., Ng, T.H. & Morales, M. (2011) Mesocorticolimbic glutamatergic pathway. J. Neurosci., 31, 8476-8490.
42. Yetnikoff, L., Lavezzi, H.N., Reichard, R.A. & Zahm, D.S. (2014) An update on the connections of the ventral mesencephalic dopaminergic complex. Neuroscience, 282C, 23-48.
43. van Zessen, R., Phillips, J.L., Budygin, E.A. & Stuber, G.D. (2012) Activation of VTA GABA neurons disrupts reward consumption. Neuron, 73, 1184-1194.