GABAergic and glutamatergic efferents of the mouse ventral tegmental area

Journal of Comparative Neurology

Volumn 522, Issue 14, 2014, Pages 3308-3334

  Taylor, Seth R ^a   Badurek, Sylvia ^b,e   Dileone, Ralph J ^a   Nashmi, Raad ^c   Minichiello, Liliana ^b,d   Picciotto, Marina R ^a  

^a YALE UNIVERSITY   (United States)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY EMBL   (Italy)

^c UNIVERSITY OF VICTORIA   (Canada)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e Department of Pharmacology University of Oxford ^*  (Austria)

Author keywords

AB_10013483; AB_10807945; AB_1091086; AB_1640532; AB_2079751; AB_2301998; AB_2311977; AB_300798; AB_390204; AB_90755; Dopamine; Lateral habenula; Mesolimbic system; Nif 0000 30467; Retrograde; Ventral pallidum; VGluT2

Indexed keywords

4 AMINOBUTYRIC ACID; CHOLINE ACETYLTRANSFERASE; GLUCOSE TRANSPORTER 2; GLUTAMATE DECARBOXYLASE 67; 2-HYDROXY-4,4'-DIAMIDINOSTILBENE, METHANESULFONATE SALT; 4 AMINOBUTYRIC ACID RECEPTOR; GLUTAMATE DECARBOXYLASE; GLUTAMATE DECARBOXYLASE 1; GLUTAMATE DECARBOXYLASE 2; GLUTAMIC ACID DERIVATIVE; PHOTOPROTEIN; SLC17A6 PROTEIN, MOUSE; STILBAMIDINE; SUBSTANCE P; TYROSINE 3 MONOOXYGENASE; VESICULAR GLUTAMATE TRANSPORTER 2; VESICULAR INHIBITORY AMINO ACID TRANSPORTER; VIAAT PROTEIN, MOUSE;

AMYGDALOID NUCLEUS; ARTICLE; BRAIN FUNCTION; DOPAMINERGIC NERVE CELL; DOPAMINERGIC SYSTEM; DORSAL RAPHE NUCLEUS; EFFERENT NERVE; GABAERGIC SYSTEM; GLOBUS PALLIDUS; HABENULA; IMMUNOHISTOCHEMISTRY; LATERAL HYPOTHALAMUS; LIMBIC SYSTEM; NERVE FIBER TRANSPORT; NEUROANATOMICAL TRACT TRACING; NONHUMAN; NUCLEOTIDE SEQUENCE; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETROGRADE NERVE FIBER TRANSPORT; REWARD; THALAMUS; VENTRAL TEGMENTUM; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; CELL COUNT; CYTOLOGY; DEPENDOPARVOVIRUS; GENETICS; METABOLISM; MOUSE; PHYSIOLOGY; TRANSGENIC MOUSE;

ANIMALS; CELL COUNT; CHOLINE O-ACETYLTRANSFERASE; DEPENDOVIRUS; EFFERENT PATHWAYS; GABAERGIC NEURONS; GLUTAMATE DECARBOXYLASE; GLUTAMATES; LUMINESCENT PROTEINS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; STILBAMIDINES; SUBSTANCE P; TYROSINE 3-MONOOXYGENASE; VENTRAL TEGMENTAL AREA; VESICULAR GLUTAMATE TRANSPORT PROTEIN 2; VESICULAR INHIBITORY AMINO ACID TRANSPORT PROTEINS;

EID: 84904489272     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23603     Document Type: Article

References (61)

1. Bocklisch C, Pascoli V, Wong JC, House DR, Yvon C, de Roo M, Tan KR, Luscher C. 2013. Cocaine disinhibits dopamine neurons by potentiation of GABA transmission in the ventral tegmental area. Science 341:1521-1525.
2. Brown MT, Tan KR, O'Connor EC, Nikonenko I, Muller D, Luscher C. 2012. Ventral tegmental area GABA projections pause accumbal cholinergic interneurons to enhance associative learning. Nature 492:452-456.
3. Carr DB, Sesack SR. 2000a. GABA-containing neurons in the rat ventral tegmental area project to the prefrontal cortex. Synapse 38:114-123.
4. Carr DB, Sesack SR. 2000b. Projections from the rat prefrontal cortex to the ventral tegmental area: target specificity in the synaptic associations with mesoaccumbens and mesocortical neurons. J Neurosci 20:3864-3873.
5. Chuhma N, Choi WY, Mingote S, Rayport S. 2009. Dopamine neuron glutamate cotransmission: frequency-dependent modulation in the mesoventromedial projection. Neuroscience 164:1068-1083.
6. Cohen JY, Haesler S, Vong L, Lowell BB, Uchida N. 2012. Neuron-type-specific signals for reward and punishment in the ventral tegmental area. Nature 482:85-88.
7. Del-Fava F, Hasue RH, Ferreira JG, Shammah-Lagnado SJ. 2007. Efferent connections of the rostral linear nucleus of the ventral tegmental area in the rat. Neuroscience 145:1059-1076.
8. Di Chiara G, Imperato A. 1988. Drugs abused by humans preferentially increase synaptic dopamine concentrations in the mesolimbic system of freely moving rats. Proc Natl Acad Sci U S A 85:5274-5278.
9. Dobi A, Margolis EB, Wang HL, Harvey BK, Morales M. 2010. Glutamatergic and nonglutamatergic neurons of the ventral tegmental area establish local synaptic contacts with dopaminergic and nondopaminergic neurons. J Neurosci 30:218-229.
10. Esclapez M, Tillakaratne NJ, Tobin AJ, Houser CR. 1993. Comparative localization of mRNAs encoding two forms of glutamic acid decarboxylase with nonradioactive in situ hybridization methods. J Comp Neurol 331:339-362.
11. Fields HL, Hjelmstad GO, Margolis EB, Nicola SM. 2007. Ventral tegmental area neurons in learned appetitive behavior and positive reinforcement. Annu Rev Neurosci 30:289-316.
12. Geisler S, Zahm DS. 2005. Afferents of the ventral tegmental area in the rat-anatomical substratum for integrative functions. J Comp Neurol 490:270-294.
13. Gervasoni D, Peyron C, Rampon C, Barbagli B, Chouvet G, Urbain N, Fort P, Luppi PH. 2000. Role and origin of the GABAergic innervation of dorsal raphe serotonergic neurons. J Neurosci 20:4217-4225.
14. Gorelova N, Mulholland PJ, Chandler LJ, Seamans JK. 2012. The glutamatergic component of the mesocortical pathway emanating from different subregions of the ventral midbrain. Cereb Cortex 22:327-336.
15. Gruber C, Kahl A, Lebenheim L, Kowski A, Dittgen A, Veh RW. 2007. Dopaminergic projections from the VTA substantially contribute to the mesohabenular pathway in the rat. Neurosci Lett 427:165-170.
16. Hnasko TS, Chuhma N, Zhang H, Goh GY, Sulzer D, Palmiter RD, Rayport S, Edwards RH. 2010. Vesicular glutamate transport promotes dopamine storage and glutamate corelease in vivo. Neuron 65:643-656.
17. Hnasko TS, Hjelmstad GO, Fields HL, Edwards RH. 2012. Ventral tegmental area glutamate neurons: electrophysiological properties and projections. J Neurosci 32:15076-15085.
18. Hong S, Jhou TC, Smith M, Saleem KS, Hikosaka O. 2011. Negative reward signals from the lateral habenula to dopamine neurons are mediated by rostromedial tegmental nucleus in primates. J Neurosci 31:11457-11471.
19. Hur EE, 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.
20. Ikemoto S. 2010. Brain reward circuitry beyond the mesolimbic dopamine system: a neurobiological theory. Neurosci Biobehav Rev 35:129-150.
21. Jhou TC, Geisler S, Marinelli M, Degarmo BA, Zahm DS. 2009. The mesopontine rostromedial tegmental nucleus: a structure targeted by the lateral habenula that projects to the ventral tegmental area of Tsai and substantia nigra compacta. J Comp Neurol 513:566-596.
22. Johnson SW, North RA. 1992. Opioids excite dopamine neurons by hyperpolarization of local interneurons. J Neurosci 12:483-488.
23. 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.
24. Kirouac GJ, Li S, Mabrouk G. 2004. GABAergic projection from the ventral tegmental area and substantia nigra to the periaqueductal gray region and the dorsal raphe nucleus. J Comp Neurol 469:170-184.
25. 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.
26. Klitenick MA, Deutch AY, Churchill L, Kalivas PW. 1992. Topography and functional role of dopaminergic projections from the ventral mesencephalic tegmentum to the ventral pallidum. Neuroscience 50:371-386.
27. Lammel S, Hetzel A, Hackel O, Jones I, Liss B, Roeper J. 2008. Unique properties of mesoprefrontal neurons within a dual mesocorticolimbic dopamine system. Neuron 57:760-773.
28. Lammel S, Ion DI, Roeper J, Malenka RC. 2011. Projection-specific modulation of dopamine neuron synapses by aversive and rewarding stimuli. Neuron 70:855-862.
29. Lassen MB, Brown JE, Stobbs SH, Gunderson SH, Maes L, Valenzuela CF, Ray AP, Henriksen SJ, Steffensen SC. 2007. Brain stimulation reward is integrated by a network of electrically coupled GABA neurons. Brain Res 1156:46-58.
30. Lavin A, Nogueira L, Lapish CC, Wightman RM, Phillips PE, Seamans JK. 2005. Mesocortical dopamine neurons operate in distinct temporal domains using multimodal signaling. J Neurosci 25:5013-5023.
31. Laviolette SR, van der Kooy D. 2003. Blockade of mesolimbic dopamine transmission dramatically increases sensitivity to the rewarding effects of nicotine in the ventral tegmental area. Mol Psychiatry 8:50-59.
32. Laviolette SR, Alexson TO, van der Kooy D. 2002. Lesions of the tegmental pedunculopontine nucleus block the rewarding effects and reveal the aversive effects of nicotine in the ventral tegmental area. J Neurosci 22:8653-8660.
33. Li YQ, Takada M, Shinonaga Y, Mizuno N. 1993. The sites of origin of dopaminergic afferent fibers to the lateral habenular nucleus in the rat. J Comp Neurol 333:118-133.
34. Mansvelder HD, McGehee DS. 2002. Cellular and synaptic mechanisms of nicotine addiction. J Neurobiol 53:606-617.
35. McBride WJ, Murphy JM, Ikemoto S. 1999. Localization of brain reinforcement mechanisms: intracranial self-administration and intracranial place-conditioning studies. Behav Brain Res 101:129-152.
36. Mitrovic I, Napier TC. 2002. Mu and kappa opioid agonists modulate ventral tegmental area input to the ventral pallidum. Eur J Neurosci 15:257-268.
37. Nair-Roberts RG, Chatelain-Badie SD, Benson E, White-Cooper H, Bolam JP, Ungless MA. 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.
38. Ohtsuka N, Badurek S, Busslinger M, Benes FM, Minichiello L, Rudolph U. 2013. GABAergic neurons regulate lateral ventricular development via transcription factor Pax5. Genesis 51:234-245.
39. Olson VG, Nestler EJ. 2007. Topographical organization of GABAergic neurons within the ventral tegmental area of the rat. Synapse 61:87-95.
40. Omelchenko N, Sesack SR. 2009. Ultrastructural analysis of local collaterals of rat ventral tegmental area neurons: GABA phenotype and synapses onto dopamine and GABA cells. Synapse 63:895-906.
41. Paxinos G, Franklin KBJ, Franklin KBJ. 2001. The mouse brain in stereotaxic coordinates. San Diego: Academic Press.
42. Pirot S, Godbout R, Mantz J, Tassin JP, Glowinski J, Thierry AM. 1992. Inhibitory effects of ventral tegmental area stimulation on the activity of prefrontal cortical neurons: evidence for the involvement of both dopaminergic and GABAergic components. Neuroscience 49:857-865.
43. Ruggerio DA, Giuliano R, Anwar M, Stornetta R, Reis DJ. 1990. Anatomical substrates of cholinergic-autonomic regulation in the rat. J Comp Neurol 292:1-53.
44. Stamatakis AM, Jennings JH, Ung RL, Blair GA, Weinberg RJ, Neve RL, Boyce F, Mattis J, Ramakrishnan C, Deisseroth K, Stuber GD. 2013. A unique population of ventral tegmental area neurons inhibits the lateral habenula to promote reward. Neuron 80:1039-1053.
45. Steffensen SC, Svingos AL, Pickel VM, Henriksen SJ. 1998. Electrophysiological characterization of GABAergic neurons in the ventral tegmental area. J Neurosci 18:8003-8015.
46. Stuber GD, Hnasko TS, Britt JP, Edwards RH, Bonci A. 2010. Dopaminergic terminals in the nucleus accumbens but not the dorsal striatum corelease glutamate. J Neurosci 30:8229-8233.
47. Swanson LW. 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.
48. Szabo B, Siemes S, Wallmichrath I. 2002. Inhibition of GABAergic neurotransmission in the ventral tegmental area by cannabinoids. Eur J Neurosci 15:2057-2061.
49. Tamamaki N, Yanagawa Y, Tomioka R, Miyazaki J, Obata K, Kaneko T. 2003. Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse. J Comp Neurol 467:60-79.
50. Tan KR, Brown M, Labouebe G, Yvon C, Creton C, Fritschy JM, Rudolph U, Luscher C. 2010. Neural bases for addictive properties of benzodiazepines. Nature 463:769-774.
51. Tan KR, Yvon C, Turiault M, Mirzabekov JJ, Doehner J, Labouebe G, Deisseroth K, Tye KM, Luscher C. 2012. GABA neurons of the VTA drive conditioned place aversion. Neuron 73:1173-1183.
52. Tecuapetla F, Patel JC, Xenias H, English D, Tadros I, Shah F, Berlin J, Deisseroth K, Rice ME, Tepper JM, Koos T. 2010. Glutamatergic signaling by mesolimbic dopamine neurons in the nucleus accumbens. J Neurosci 30:7105-7110.
53. Tolu S, Eddine R, Marti F, David V, Graupner M, Pons S, Baudonnat M, Husson M, Besson M, Reperant C, Zemdegs J, Pages C, Hay YA, Lambolez B, Caboche J, Gutkin B, Gardier AM, Changeux JP, Faure P, Maskos U. 2013. Co-activation of VTA DA and GABA neurons mediates nicotine reinforcement. Mol Psychiatry 18:382-393.
54. Van Bockstaele EJ, Pickel VM. 1995. GABA-containing neurons in the ventral tegmental area project to the nucleus accumbens in rat brain. Brain Res 682:215-221.
55. van Zessen R, Phillips JL, Budygin EA, Stuber GD. 2012. Activation of VTA GABA neurons disrupts reward consumption. Neuron 73:1184-1194.
56. Vong L, Ye C, Yang Z, Choi B, Chua S Jr, Lowell BB. 2011. Leptin action on GABAergic neurons prevents obesity and reduces inhibitory tone to POMC neurons. Neuron 71:142-154.
57. Wang X, Sun QQ. 2012. Characterization of axo-axonic synapses in the piriform cortex of Mus musculus. J Comp Neurol 520:832-847.
58. Watabe-Uchida M, Zhu L, Ogawa SK, Vamanrao A, Uchida N. 2012. Whole-brain mapping of direct inputs to midbrain dopamine neurons. Neuron 74:858-873.
59. Wise RA. 1996. Addictive drugs and brain stimulation reward. Annu Rev Neurosci 19:319-340.
60. Yamaguchi T, Sheen W, Morales M. 2007. Glutamatergic neurons are present in the rat ventral tegmental area. Eur J Neurosci 25:106-118.
61. Yamaguchi T, Wang HL, Li X, Ng TH, Morales M. 2011. Mesocorticolimbic glutamatergic pathway. J Neurosci 31:8476-8490.