Dopamine inhibits GABAA currents in ventral tegmental area dopamine neurons via activation of presynaptic G-protein coupled inwardly-rectifying potassium channels

Neuroscience

Volumn 165, Issue 4, 2010, Pages 1159-1169

  Michaeli, A ^a   Yaka, R ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

disinhibition; dopamine; GABAA receptor; GIRK; psychostimulants; reward circuit

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID B RECEPTOR; DOPAMINE; DOPAMINE 2 RECEPTOR; DOPAMINE 2 RECEPTOR LIKE RECEPTOR; G PROTEIN COUPLED INWARDLY RECTIFYING POTASSIUM CHANNEL; UNCLASSIFIED DRUG;

4 AMINOBUTYRIC ACID RELEASE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; EXTRACELLULAR CALCIUM; GABAERGIC TRANSMISSION; INHIBITORY POSTSYNAPTIC POTENTIAL; MALE; NERVE EXCITABILITY; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; RAT; VENTRAL TEGMENTUM;

ANIMALS; CALCIUM; DOPAMINE; EVOKED POTENTIALS; EXTRACELLULAR SPACE; G PROTEIN-COUPLED INWARDLY-RECTIFYING POTASSIUM CHANNELS; GAMMA-AMINOBUTYRIC ACID; INHIBITORY POSTSYNAPTIC POTENTIALS; MALE; NEURAL INHIBITION; NEURONS; PRESYNAPTIC TERMINALS; RATS; RATS, INBRED STRAINS; RECEPTORS, DOPAMINE D2; RECEPTORS, GABA-A; RECEPTORS, GABA-B; SYNAPTIC TRANSMISSION; VENTRAL TEGMENTAL AREA;

EID: 73649211098     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2009.11.045     Document Type: Article

References (56)

1. Armstrong C.M., Swenson Jr. R.P., and Taylor S.R. Block of squid axon K channels by internally and externally applied barium ions. J Gen Physiol 80 (1982) 663-682
2. Beart P.M., and McDonald D. 5-Hydroxytryptamine and 5-hydroxytryptaminergic-dopaminergic interactions in the ventral tegmental area of rat brain. J Pharm Pharmacol 34 (1982) 591-593
3. Bradberry C.W., and Roth R.H. Cocaine increases extracellular dopamine in rat nucleus accumbens and ventral tegmental area as shown by in vivo microdialysis. Neurosci Lett 103 (1989) 97-102
4. Brancucci A., Berretta N., Mercuri N.B., and Francesconi W. Presynaptic modulation of spontaneous inhibitory postsynaptic currents by gamma-hydroxybutyrate in the substantia nigra pars compacta. Neuropsychopharmacology 29 (2004) 537-543
5. Cameron D.L., and Williams J.T. Dopamine D1 receptors facilitate transmitter release. Nature 366 (1993) 344-347
6. Cameron D.L., and Williams J.T. Cocaine inhibits GABA release in the VTA through endogenous 5-HT. J Neurosci 14 (1994) 6763-6767
7. Choi S., and Lovinger D.M. Decreased probability of neurotransmitter release underlies striatal long-term depression and postnatal development of corticostriatal synapses. Proc Natl Acad Sci U S A 94 (1997) 2665-2670
8. Civelli O., Bunzow J.R., and Grandy D.K. Molecular diversity of the dopamine receptors. Annu Rev Pharmacol Toxicol 33 (1993) 281-307
9. Cruz H.G., Ivanova T., Lunn M.L., Stoffel M., Slesinger P.A., and Luscher C. Bi-directional effects of GABA(B) receptor agonists on the mesolimbic dopamine system. Nat Neurosci 7 (2004) 153-159
10. Dascal N. Signalling via the G protein-activated K+ channels. Cell Signal 9 (1997) 551-573
11. Davies C.H., Davies S.N., and Collingridge G.L. Paired-pulse depression of monosynaptic GABA-mediated inhibitory postsynaptic responses in rat hippocampus. J Physiol 424 (1990) 513-531
12. Di Chiara G., and Bassareo V. Reward system and addiction: what dopamine does and doesn't do. Curr Opin Pharmacol 7 (2007) 69-76
13. Diaz J., Pilon C., Le Foll B., Gros C., Triller A., Schwartz J.C., and Sokoloff P. Dopamine D3 receptors expressed by all mesencephalic dopamine neurons. J Neurosci 20 (2000) 8677-8684
14. Djaldetti R., and Melamed E. New therapies for Parkinson's disease. J Neurol 248 (2001) 357-362
15. Fields H.L., Hjelmstad G.O., Margolis E.B., and Nicola S.M. Ventral tegmental area neurons in learned appetitive behavior and positive reinforcement. Annu Rev Neurosci 30 (2007) 289-316
16. Geisler S., Derst C., Veh R.W., and Zahm D.S. Glutamatergic afferents of the ventral tegmental area in the rat. J Neurosci 27 (2007) 5730-5743
17. Gifford A.N., and Johnson K.M. Comparison of the role of local anesthetic properties with dopamine uptake blockade in the inhibition of striatal and nucleus accumbens [3H]acetylcholine release by cocaine. J Pharmacol Exp Ther 263 (1992) 757-761
18. Gonzalez-Islas C., and Hablitz J.J. Dopamine inhibition of evoked IPSCs in rat prefrontal cortex. J Neurophysiol 86 (2001) 2911-2918
19. Hua S.Y., Raciborska D.A., Trimble W.S., and Charlton M.P. Different VAMP/synaptobrevin complexes for spontaneous and evoked transmitter release at the crayfish neuromuscular junction. J Neurophysiol 80 (1998) 3233-3246
20. Jin W., and Lu Z. A novel high-affinity inhibitor for inward-rectifier K+ channels. Biochemistry 37 (1998) 13291-13299
21. Johnson S.W., and North R.A. Two types of neurone in the rat ventral tegmental area and their synaptic inputs. J Physiol 450 (1992) 455-468
22. Johnson S.W., and North R.A. Opioids excite dopamine neurons by hyperpolarization of local interneurons. J Neurosci 12 (1992) 483-488
23. Kalivas P.W., and Duffy P. A comparison of axonal and somatodendritic dopamine release using in vivo dialysis. J Neurochem 56 (1991) 961-967
24. Kalivas P.W., and Volkow N.D. The neural basis of addiction: a pathology of motivation and choice. Am J Psychiatry 162 (2005) 1403-1413
25. Kalivas P.W., Bourdelais A., Abhold R., and Abbott L. Somatodendritic release of endogenous dopamine: in vivo dialysis in the A10 dopamine region. Neurosci Lett 100 (1989) 215-220
26. Koga E., and Momiyama T. Presynaptic dopamine D2-like receptors inhibit excitatory transmission onto rat ventral tegmental dopaminergic neurones. J Physiol 523 Pt 1 (2000) 163-173
27. Kuhar M.J., Ritz M.C., and Boja J.W. The dopamine hypothesis of the reinforcing properties of cocaine. Trends Neurosci 14 (1991) 299-302
28. Kuzhikandathil E.V., and Oxford G.S. Classic D1 dopamine receptor antagonist R-(+)-7-chloro-8-hydroxy-3-methyl-1-phenyl-2,3,4,5-tetrahydro-1H-3-benzaze pine hydrochloride (SCH23390) directly inhibits G protein-coupled inwardly rectifying potassium channels. Mol Pharmacol 62 (2002) 119-126
29. Labouebe G., Lomazzi M., Cruz H.G., Creton C., Lujan R., Li M., Yanagawa Y., Obata K., Watanabe M., Wickman K., Boyer S.B., Slesinger P.A., and Luscher C. RGS2 modulates coupling between GABAB receptors and GIRK channels in dopamine neurons of the ventral tegmental area. Nat Neurosci 10 (2007) 1559-1568
30. Lantin Le Boulch N., Truong-Ngoc N.A., and Gauchy C. Role of dendritic dopamine of the substantia nigra in the modulation of nigrocollicular gamma-aminobutyric acid release: in vivo studies in the rat. J Neurochem 57 (1991) 1080-1083
31. Leone P., Pocock D., and Wise R.A. Morphine-dopamine interaction: ventral tegmental morphine increases nucleus accumbens dopamine release. Pharmacol Biochem Behav 39 (1991) 469-472
32. Levant B., Grigoriadis D.E., and DeSouza E.B. Characterization of [3H]quinpirole binding to D2-like dopamine receptors in rat brain. J Pharmacol Exp Ther 262 (1992) 929-935
33. Li Y., and van den Pol A.N. Direct and indirect inhibition by catecholamines of hypocretin/orexin neurons. J Neurosci 25 (2005) 173-183
34. Liu Q.S., Pu L., and Poo M.M. Repeated cocaine exposure in vivo facilitates LTP induction in midbrain dopamine neurons. Nature 437 (2005) 1027-1031
35. Lomazzi M., Slesinger P.A., and Luscher C. Addictive drugs modulate GIRK-channel signaling by regulating RGS proteins. Trends Pharmacol Sci 29 (2008) 544-549
36. Mennerick S., and Zorumski C.F. Paired-pulse modulation of fast excitatory synaptic currents in microcultures of rat hippocampal neurons. J Physiol 488 Pt 1 (1995) 85-101
37. Missale C., Nash S.R., Robinson S.W., Jaber M., and Caron M.G. Dopamine receptors: from structure to function. Physiol Rev 78 (1998) 189-225
38. Mullner C., Yakubovich D., Dessauer C.W., Platzer D., and Schreibmayer W. Single channel analysis of the regulation of GIRK1/GIRK4 channels by protein phosphorylation. Biophys J 84 (2003) 1399-1409
39. Nestler E.J. The neurobiology of cocaine addiction. Sci Pract Perspect 3 (2005) 4-10
40. Nirenberg M.J., Chan J., Vaughan R.A., Uhl G.R., Kuhar M.J., and Pickel V.M. Immunogold localization of the dopamine transporter: an ultrastructural study of the rat ventral tegmental area. J Neurosci 17 (1997) 5255-5262
41. Pan B., Hillard C.J., and Liu Q.S. D2 dopamine receptor activation facilitates endocannabinoid-mediated long-term synaptic depression of GABAergic synaptic transmission in midbrain dopamine neurons via cAMP-protein kinase A signaling. J Neurosci 28 (2008) 14018-14030
42. Pan B., Hillard C.J., and Liu Q.S. Endocannabinoid signaling mediates cocaine-induced inhibitory synaptic plasticity in midbrain dopamine neurons. J Neurosci 28 (2008) 1385-1397
43. Radnikow G., and Misgeld U. Dopamine D1 receptors facilitate GABAA synaptic currents in the rat substantia nigra pars reticulata. J Neurosci 18 (1998) 2009-2016
44. Sadja R., Alagem N., and Reuveny E. Gating of GIRK channels: details of an intricate, membrane-delimited signaling complex. Neuron 39 (2003) 9-12
45. Schilstrom B., Yaka R., Argilli E., Suvarna N., Schumann J., Chen B.T., Carman M., Singh V., Mailliard W.S., Ron D., and Bonci A. Cocaine enhances NMDA receptor-mediated currents in ventral tegmental area cells via dopamine D5 receptor-dependent redistribution of NMDA receptors. J Neurosci 26 (2006) 8549-8558
46. Sesack S.R., Aoki C., and Pickel V.M. Ultrastructural localization of D2 receptor-like immunoreactivity in midbrain dopamine neurons and their striatal targets. J Neurosci 14 (1994) 88-106
47. Sosulina L., Schwesig G., Seifert G., and Pape H.C. Neuropeptide Y activates a G-protein-coupled inwardly rectifying potassium current and dampens excitability in the lateral amygdala. Mol Cell Neurosci 39 (2008) 491-498
48. Stanfield P.R., Nakajima S., and Nakajima Y. Constitutively active and G-protein coupled inward rectifier K+ channels: Kir20 and Kir30. Rev Physiol Biochem Pharmacol 145 (2002) 47-179
49. Steffensen S.C., Taylor S.R., Horton M.L., Barber E.N., Lyle L.T., Stobbs S.H., and Allison D.W. Cocaine disinhibits dopamine neurons in the ventral tegmental area via use-dependent blockade of GABA neuron voltage-sensitive sodium channels. Eur J Neurosci 28 (2008) 2028-2040
50. Sugita S., Johnson S.W., and North R.A. Synaptic inputs to GABAA and GABAB receptors originate from discrete afferent neurons. Neurosci Lett 134 (1992) 207-211
51. Taverna S., Canciani B., and Pennartz C.M. Dopamine D1-receptors modulate lateral inhibition between principal cells of the nucleus accumbens. J Neurophysiol 93 (2005) 1816-1819
52. Tseng K.Y., and O'Donnell P. D2 dopamine receptors recruit a GABA component for their attenuation of excitatory synaptic transmission in the adult rat prefrontal cortex. Synapse 61 (2007) 843-850
53. Van der Kloot W. The regulation of quantal size. Prog Neurobiol 36 (1991) 93-130
54. Werner P., Hussy N., Buell G., Jones K.A., and North R.A. D2, D3, and D4 dopamine receptors couple to G protein-regulated potassium channels in Xenopus oocytes. Mol Pharmacol 49 (1996) 656-661
55. White F.J. Synaptic regulation of mesocorticolimbic dopamine neurons. Annu Rev Neurosci 19 (1996) 405-436
56. Witkowski G., Szulczyk B., Rola R., and Szulczyk P. D(1) dopaminergic control of G protein-dependent inward rectifier K(+) (GIRK)-like channel current in pyramidal neurons of the medial prefrontal cortex. Neuroscience 155 (2008) 53-63