Glutamate and dopamine transmission from midbrain dopamine neurons share similar release properties but are differentially affected by cocaine

Journal of Neuroscience

Volumn 34, Issue 9, 2014, Pages 3183-3192

  Adrover, Martín F ^a   Shin, Jung Hoon ^a   Alvarez, Veronica A ^a  

^a NATIONAL INSTITUTE ON ALCOHOL ABUSE AND ALCOHOLISM   (United States)

Author keywords

Co release; Cocaine; D2 receptors; Dopamine; Feedback inhibition; Glutamate

Indexed keywords

2 3 DIHYDROXY 6 NITRO 7 SULFONYL BENZO[F]QUINOXALINE; 4 (3 PHOSPHONOPROPYL) 2 PIPERAZINECARBOXYLIC ACID; AMPA RECEPTOR; BENZO [F] QUINOXALINE DERIVATIVE; COCAINE; DOPAMINE 2 RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NOMIFENSINE; PRESYNAPTIC RECEPTOR; QUINPIROLE; SULPIRIDE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYCLIC POTENTIOMETRY; DOPAMINERGIC NERVE CELL; DOPAMINERGIC TRANSMISSION; ELECTROPHYSIOLOGY; ELECTROSTIMULATION; GENE DELETION; GLUTAMATERGIC TRANSMISSION; MALE; MESENCEPHALON; MOUSE; NEUROTRANSMISSION; NONHUMAN; OPTOGENETICS; PRIORITY JOURNAL; SYNAPTIC POTENTIAL;

CO-RELEASE; COCAINE; D2 RECEPTORS; DOPAMINE; FEEDBACK INHIBITION; GLUTAMATE;

ANIMALS; DEPENDOVIRUS; DOPAMINE AGENTS; DOPAMINE PLASMA MEMBRANE TRANSPORT PROTEINS; DOPAMINE UPTAKE INHIBITORS; DOPAMINERGIC NEURONS; EXCITATORY AMINO ACID ANTAGONISTS; GLUTAMIC ACID; GREEN FLUORESCENT PROTEINS; MALE; MESENCEPHALON; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUTATION; QUINOXALINES; RECEPTORS, DOPAMINE D2; RHODOPSIN; SYNAPTIC TRANSMISSION;

EID: 84894465617     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4958-13.2014     Document Type: Article

References (49)

1. Alsiö J, Nordenankar K, Arvidsson E, Birgner C, Mahmoudi S, Halbout B, Smith C, Fortin GM, Olson L, Descarries L, Trudeau LÉ, Kullander K, Lévesque D, Wallén-MackenzieA (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. CrossRef Medline
2. Bäckman CM, Malik N, Zhang Y, Shan L, Grinberg A, Hoffer BJ, Westphal H, Tomac AC (2006) Characterization of a mouse strain expressing Cre recombinase from the 3́ untranslated region of the dopamine transporter locus. Genesis 44:383-390. CrossRef Medline
3. Bello EP, Mateo Y, Gelman DM, Noaín D, Shin JH, Low MJ, Alvarez VA, Lovinger DM, Rubinstein M (2011) Cocaine supersensitivity and enhanced motivation for reward in mice lacking dopamine D2 autoreceptors. Nat Neurosci 14:1033-1038. CrossRef Medline
4. Bérubé-Carrière N, Riad M, Dal Bo G, Lévesque D, Trudeau LE, Descarries L (2009) The dual dopamine-glutamate phenotype of growing mesencephalic neurons regresses in mature rat brain. J Comp Neurol 517:873-891. CrossRef Medline
5. Bérubé-Carrière N, Guay G, Fortin GM, Kullander K, Olson L, Wallén-Mackenzie Å, Trudeau LE, Descarries L (2012) Ultrastructural characterization of the mesostriatal dopamine innervation in mice, including two mouse lines of conditional VGLUT2 knockout in dopamine neurons. Eur J Neurosci 35:527-538. CrossRef Medline
6. Birgner C, Nordenankar K, Lundblad M, Mendez JA, Smith C, le Grevès M, Galter D, Olson L, Fredriksson A, Trudeau LE, Kullander K, Wallén-Mackenzie A (2010) VGLUT2 in dopamine neurons is required for psychostimulant-induced behavioral activation. Proc Natl Acad SciU S A 107:389-394. CrossRef Medline
7. Budygin EA, John CE, Mateo Y, Jones SR (2002) Lack of cocaine effect on dopamine clearance in the core and shell of the nucleus accumbens of dopamine transporter knock-out mice. J Neurosci 22:RC222(1-4). Medline
8. Cachope R, Mateo Y, Mathur BN, Irving J, Wang HL, Morales M, Lovinger DM, Cheer JF (2012) Selective activation of cholinergic interneurons enhances accumbal phasic dopamine release: setting the tone for reward processing. Cell Rep 2:33-41. CrossRef Medline
9. Chuhma N, Zhang H, Masson J, Zhuang X, Sulzer D, Hen R, Rayport S (2004) Dopamine neurons mediate a fast excitatory signal via their glutamatergic synapses. J Neurosci 24:972-981. CrossRef Medline
10. Cragg SJ, Greenfield SA (1997) Differential autoreceptor control of somatodendritic and axon terminal dopamine release in substantia nigra, ventral tegmental area, and striatum. J Neurosci 17:5738-5746. Medline
11. Dal Bo G, St-Gelais F, Danik M, Williams S, Cotton M, Trudeau LE (2004) Dopamine neurons in culture express VGLUT2 explaining their capacity to release glutamate at synapses in addition to dopamine. J Neurochem 88:1398-1405. CrossRef Medline
12. Dal Bo G, Bérubé-Carrière N, Mendez JA, Leo D, Riad M, Descarries L, Lévesque D, Trudeau LE (2008) Enhanced glutamatergic phenotype of mesencephalic dopamine neurons after neonatal 6-hydroxydopamine lesion. Neuroscience 156:59-70. CrossRef Medline
13. DeBoer P, Heeringa MJ, Abercrombie ED (1996) Spontaneous release of acetylcholine in striatum is preferentially regulated by inhibitory dopamine D2 receptors. Eur J Pharmacol 317:257-262. CrossRef Medline
14. Di Chiara G, Bassareo V, Fenu S, De Luca MA, Spina L, Cadoni C, Acquas E, Carboni E, Valentini V, Lecca D (2004) Dopamine and drug addiction: the nucleus accumbens shell connection. Neuropharmacology 47 [Suppl 1]:227-241.
15. Dunwiddie TV, Proctor WR, Tyma J (1988) Local anaesthetic actions of cocaine: effects on excitatory and inhibitory synaptic responses in the hippocampus in vitro. Br J Pharmacol 95:1117-1124. CrossRef Medline
16. Franklin KBJ, PaxinosG (2007) The mouse brain in stereotaxic coordinates, Ed 3. Amsterdam: Elsevier.
17. Gifford AN, Johnson KM (1992) Effect of chronic cocaine treatment on D2 receptors regulating the release of dopamine and acetylcholine in the nucleus accumbens and striatum. Pharmacol Biochem Behav 41:841-846. CrossRef Medline
18. Grueter BA, Brasnjo G, Malenka RC (2010) Postsynaptic TRPV1 triggers cell type-specific long-term depression in the nucleus accumbens. Nat Neurosci 13:1519-1525. CrossRef Medline
19. 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. CrossRef Medline
20. Ikemoto S, Bonci A (2014) Neurocircuitry of drug reward. Neuropharmacology 76:329-341. CrossRef Medline
21. John CE, Jones SR (2007) Voltammetric characterization of the effect of monoamine uptake inhibitors and releasers on dopamine and serotonin uptake in mouse caudate-putamen and substantia nigra slices. Neuropharmacology 52:1596-1605. CrossRef Medline
22. Jones SR, Garris PA, Wightman RM (1995) Different effects of cocaine and nomifensine on dopamine uptake in the caudate-putamen and nucleus accumbens. J Pharmacol Exp Ther 274:396-403. Medline
23. Kalivas PW (2004) Glutamate systems in cocaine addiction. Curr Opin Pharmacol 4:23-29. CrossRef Medline
24. 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. CrossRef Medline
25. Kennedy RT, Jones SR, Wightman RM (1992) Dynamic observation of dopamine autoreceptor effects in rat striatal slices. J Neurochem 59:449-455. CrossRef Medline
26. Kile BM, Guillot TS, Venton BJ, Wetsel WC, Augustine GJ, Wightman RM (2010) Synapsins differentially control dopamine and serotonin release. J Neurosci 30:9762-9770. CrossRef Medline
27. Lee TH, Balu R, Davidson C, Ellinwood EH (2001) Differential time-course profiles of dopamine release and uptake changes induced by three dopamine uptake inhibitors. Synapse 41:301-310. CrossRef Medline
28. Lee TH, Gee KR, Davidson C, EllinwoodEH (2002) Direct, real-time assessment of dopamine release autoinhibition in the rat caudate-putamen. Neuroscience 112:647-654. CrossRef Medline
29. Mendez JA, Bourque MJ, Dal Bo G, Bourdeau ML, Danik M, Williams S, Lacaille JC, Trudeau LE (2008) Developmental and target-dependent regulation of vesicular glutamate transporter expression by dopamine neurons. J Neurosci 28:6309-6318. CrossRef Medline
30. Moss J, Ungless MA, Bolam JP (2011) Dopaminergic axons in different divisions of the adult rat striatal complex do not express vesicular glutamate transporters. Eur J Neurosci 33:1205-1211. CrossRef Medline
31. Nestler EJ (2001) Molecular basis of long-term plasticity underlying addiction. Nat Rev Neurosci 2:119-128. CrossRef Medline
32. Phillips PE, Hancock PJ, Stamford JA (2002) Time window of autoreceptormediated inhibition of limbic and striatal dopamine release. Synapse 44: 15-22. CrossRef Medline
33. Rice ME, Patel JC, Cragg SJ (2011) Dopamine release in the basal ganglia. Neuroscience 198:112-137. CrossRef Medline
34. Ruetsch YA, Böni T, Borgeat A (2001) From cocaine to ropivacaine: the history of local anesthetic drugs. Curr Top Med Chem 1:175-182. CrossRef Medline
35. Self DW, Choi KH, Simmons D, Walker JR, Smagula CS (2004) Extinction training regulates neuroadaptive responses to withdrawal from chronic cocaine self-administration. Learn Mem 11:648-657. CrossRef Medline
36. Shuen JA, Chen M, Gloss B, CalakosN (2008) Drd1a-tdTomato BAC transgenic mice for simultaneous visualization of medium spiny neurons in the direct and indirect pathways of the basal ganglia. J Neurosci 28:2681-2685. CrossRef Medline
37. 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. CrossRef Medline
38. Sulzer D, Joyce MP, Lin L, Geldwert D, Haber SN, Hattori T, Rayport S (1998) Dopamine neurons make glutamatergic synapses in vitro. J Neurosci 18:4588-4602. Medline
39. 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. CrossRef Medline
40. Thomas MJ, Beurrier C, Bonci A, Malenka RC (2001) Long-term depression in the nucleus accumbens: a neural correlate of behavioral sensitization to cocaine. Nat Neurosci 4:1217-1223. CrossRef Medline
41. Threlfell S, Lalic T, Platt NJ, Jennings KA, Deisseroth K, Cragg SJ (2012) Striatal dopamine release is triggered by synchronized activity in cholinergic interneurons. Neuron 75:58-64. CrossRef Medline
42. Tritsch NX, Ding JB, Sabatini BL (2012) Dopaminergic neurons inhibit striatal output through non-canonical release of GABA. Nature 490:262-266. CrossRef Medline
43. Trout SJ, Kruk ZL (1992) Differences in evoked dopamine efflux in rat caudate putamen, nucleus accumbens and tuberculum olfactorium in the absence of uptake inhibition: influence of autoreceptors. Br J Pharmacol 106:452-458. CrossRef Medline
44. Venton BJ, Seipel AT, Phillips PE, Wetsel WC, Gitler D, Greengard P, Augustine GJ, Wightman RM (2006) Cocaine increases dopamine release by mobilization of a synapsin-dependent reserve pool. J Neurosci 26:3206-3209. CrossRef Medline
45. Wieczorek WJ, Kruk ZL (1994) A quantitative comparison on the effects of benztropine, cocaine and nomifensine on electrically evoked dopamine overflow and rate of re-uptake in the caudate putamen and nucleus accumbens in the rat brain slice. Brain Res 657:42-50. CrossRef Medline
46. Wise RA (2004) Dopamine, learning and motivation. Nat Rev Neurosci 5:483-494. CrossRef Medline
47. Yamaguchi T, Wang HL, Li X, Ng TH, Morales M (2011) Mesocorticolimbic glutamatergic pathway. J Neurosci 31:8476-8490. CrossRef Medline
48. Yamaguchi T, Wang HL, MoralesM (2013) Glutamate neurons in the substantia nigra compacta and retrorubral field. Eur J Neurosci 38:3602-3610. CrossRef Medline
49. Zhou FM, Liang Y, Dani JA (2001) Endogenous nicotinic cholinergic activity regulates dopamine release in the striatum. Nat Neurosci 4:1224-1229. CrossRef Medline