Differential role of ventral tegmental area acetylcholine and N-methyl-d-aspartate receptors in cocaine-seeking

Neuropharmacology

Volumn 75, Issue , 2013, Pages 9-18

  Solecki, Wojciech ^a   Wickham, Robert J ^a,b   Behrens, Shay ^a   Wang, Jie ^a,c   Zwerling, Blake ^a   Mason, Graeme F ^a   Addy, Nii A ^a,b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b YALE UNIVERSITY   (United States)

^c Wuhan National Laboratory for Optoelectronics   (China)

Author keywords

Acetylcholine; Drug seeking; NMDA; Nucleus accumbens; Phasic dopamine; Ventral tegmental area

Indexed keywords

2 AMINO 5 PHOSPHONOVALERIC ACID; CHOLINERGIC RECEPTOR; COCAINE; DOPAMINE; DOPAMINE 1 RECEPTOR; MECAMYLAMINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; SCOPOLAMINE;

ABSTINENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASSOCIATION; BRAIN TISSUE; COCAINE DEPENDENCE; CONTROLLED STUDY; CYCLIC POTENTIOMETRY; DOPAMINE RELEASE; DRUG SEEKING BEHAVIOR; LOCOMOTION; MALE; NERVE CELL NETWORK; NEUROMODULATION; NEUROPATHOLOGY; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; RAT; RECEPTOR OCCUPANCY; RECEPTOR UPREGULATION; VENTRAL TEGMENTUM;

ACETYLCHOLINE; DRUG-SEEKING; NMDA; NUCLEUS ACCUMBENS; PHASIC DOPAMINE; VENTRAL TEGMENTAL AREA;

ACETYLCHOLINE; ANESTHETICS, LOCAL; ANIMALS; BENZAZEPINES; CHOLINERGIC ANTAGONISTS; COCAINE; CUES; DOPAMINE; DOPAMINE AGONISTS; DRUG-SEEKING BEHAVIOR; LIDOCAINE; MALE; MECAMYLAMINE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; SCOPOLAMINE HYDROBROMIDE; TIME FACTORS; VALINE; VENTRAL TEGMENTAL AREA;

EID: 84883089266     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2013.07.001     Document Type: Article

References (62)

1. A.R. Adamantidis, H.C. Tsai, B. Boutrel, F. Zhang, G.D. Stuber, E.A. Budygin, C. Tourino, A. Bonci, K. Deisseroth, and L. de Lecea Optogenetic interrogation of dopaminergic modulation of the multiple phases of reward-seeking behavior J. Neurosci. 31 2011 10829 10835
2. S.P. Berger, S. Hall, J.D. Mickalian, M.S. Reid, C.A. Crawford, K. Delucchi, and K. Carr Haloperidol antagonism of cue-elicited cocaine craving Lancet 347 1996 504 508
3. C.D. Blaha, L.F. Allen, S. Das, W.L. Inglis, M.P. Latimer, S.R. Vincent, and P. Winn Modulation of dopamine efflux in the nucleus accumbens after cholinergic stimulation of the ventral tegmental area in intact, pedunculopontine tegmental nucleus-lesioned, and laterodorsal tegmental nucleus-lesioned rats J. Neurosci. 16 1996 714 722
4. C. Calaminus, and W. Hauber Intact discrimination reversal learning but slowed responding to reward-predictive cues after dopamine D1 and D2 receptor blockade in the nucleus accumbens of rats Psychopharmacology (Berl) 191 2007 551 566
5. B.T. Chen, M.S. Bowers, M. Martin, F.W. Hopf, A.M. Guillory, R.M. Carelli, J.K. Chou, and A. Bonci Cocaine but not natural reward self-administration nor passive cocaine infusion produces persistent LTP in the VTA Neuron 59 2008 288 297
6. K. Chergui, P.J. Charlety, H. Akaoka, C.F. Saunier, J.L. Brunet, M. Buda, T.H. Svensson, and G. Chouvet Tonic activation of NMDA receptors causes spontaneous burst discharge of rat midbrain dopamine neurons in vivo Eur. J. Neurosci. 5 1993 137 144
7. J.J. Day, M.F. Roitman, R.M. Wightman, and R.M. Carelli Associative learning mediates dynamic shifts in dopamine signaling in the nucleus accumbens Nat. Neurosci. 10 2007 1020 1028
8. A. Fink-Jensen, I. Fedorova, G. Wortwein, D.P. Woldbye, T. Rasmussen, M. Thomsen, T.G. Bolwig, K.M. Knitowski, D.L. McKinzie, M. Yamada, J. Wess, and A. Basile Role for M5 muscarinic acetylcholine receptors in cocaine addiction J. Neurosci. Res. 74 2003 91 96
9. M.B. Ghasemzadeh, P. Vasudevan, C. Giles, A. Purgianto, C. Seubert, and J.R. Mantsch Glutamatergic plasticity in medial prefrontal cortex and ventral tegmental area following extended-access cocaine self-administration Brain Res. 1413 2011 60 71
10. R.Z. Goldstein, D. Tomasi, N. Alia-Klein, J. Honorio Carrillo, T. Maloney, P.A. Woicik, R. Wang, F. Telang, and N.D. Volkow Dopaminergic response to drug words in cocaine addiction J. Neurosci. 29 2009 6001 6006
11. Y. Goto, and A.A. Grace Dopamine-dependent interactions between limbic and prefrontal cortical plasticity in the nucleus accumbens: disruption by cocaine sensitization Neuron 47 2005 255 266
12. S.E. Hemby, B. Horman, and W. Tang Differential regulation of ionotropic glutamate receptor subunits following cocaine self-administration Brain Res. 1064 2005 75 82
13. R. Ito, J.W. Dalley, S.R. Howes, T.W. Robbins, and B.J. Everitt Dissociation in conditioned dopamine release in the nucleus accumbens core and shell in response to cocaine cues and during cocaine-seeking behavior in rats J. Neurosci. 20 2000 7489 7495
14. P.W. Kalivas, and K. McFarland Brain circuitry and the reinstatement of cocaine-seeking behavior Psychopharmacology (Berl) 168 2003 44 56
15. S.T. Kitai, P.D. Shepard, J.C. Callaway, and R. Scroggs Afferent modulation of dopamine neuron firing patterns Curr. Opin. Neurobiol. 9 1999 690 697
16. H.R. Kranzler, and L.O. Bauer Bromocriptine and cocaine cue reactivity in cocaine-dependent patients Br. J. Addict. 87 1992 1537 1548
17. V. Kumaresan, M. Yuan, J. Yee, K.R. Famous, S.M. Anderson, H.D. Schmidt, and R.C. Pierce Metabotropic glutamate receptor 5 (mGluR5) antagonists attenuate cocaine priming- and cue-induced reinstatement of cocaine seeking Behav. Brain Res. 202 2009 238 244
18. S. Lammel, B.K. Lim, C. Ran, K.W. Huang, M.J. Betley, K.M. Tye, K. Deisseroth, and R.C. Malenka Input-specific control of reward and aversion in the ventral tegmental area Nature 491 2012 212 217
19. H.C. Lasseter, A.M. Wells, X. Xie, and R.A. Fuchs Interaction of the basolateral amygdala and orbitofrontal cortex is critical for drug context-induced reinstatement of cocaine-seeking behavior in rats Neuropsychopharmacology 36 2011 711 720
20. D.B. Lester, A.D. Miller, T.D. Pate, and C.D. Blaha Midbrain acetylcholine and glutamate receptors modulate accumbal dopamine release Neuroreport 19 2008 991 995
21. D.J. Lodge, and A.A. Grace The laterodorsal tegmentum is essential for burst firing of ventral tegmental area dopamine neurons Proc. Natl. Acad. Sci. U. S. A. 103 2006 5167 5172
22. E. Lof, P. Olausson, A. deBejczy, R. Stomberg, J.M. McIntosh, J.R. Taylor, and B. Soderpalm Nicotinic acetylcholine receptors in the ventral tegmental area mediate the dopamine activating and reinforcing properties of ethanol cues Psychopharmacology (Berl) 195 2007 333 343
23. L. Lu, J.W. Grimm, Y. Shaham, and B.T. Hope Molecular neuroadaptations in the accumbens and ventral tegmental area during the first 90 days of forced abstinence from cocaine self-administration in rats J. Neurochem. 85 2003 1604 1613
24. C. Luscher, and R.C. Malenka Drug-evoked synaptic plasticity in addiction: from molecular changes to circuit remodeling Neuron 69 2011 650 663
25. S.V. Mahler, R.J. Smith, and G. Aston-Jones Interactions between VTA orexin and glutamate in cue-induced reinstatement of cocaine seeking in rats Psychopharmacology (Berl) 226 4 2013 687 698
26. U. Maskos The cholinergic mesopontine tegmentum is a relatively neglected nicotinic master modulator of the dopaminergic system: relevance to drugs of abuse and pathology Br. J. Pharmacol. 153 Suppl. 1 2008 S438 S445
27. K. McFarland, and P.W. Kalivas The circuitry mediating cocaine-induced reinstatement of drug-seeking behavior J. Neurosci. 21 2001 8655 8663
28. S.M. Nicola, S.A. Taha, S.W. Kim, and H.L. Fields Nucleus accumbens dopamine release is necessary and sufficient to promote the behavioral response to reward-predictive cues Neuroscience 135 2005 1025 1033
29. P. Overton, and D. Clark Iontophoretically administered drugs acting at the N-methyl-D-aspartate receptor modulate burst firing in A9 dopamine neurons in the rat Synapse 10 1992 131 140
30. C.A. Owesson-White, J.F. Cheer, M. Beyene, R.M. Carelli, and R.M. Wightman Dynamic changes in accumbens dopamine correlate with learning during intracranial self-stimulation Proc. Natl. Acad. Sci. U. S. A. 105 2008 11957 11962
31. G. Paxinos, and C. Watson The Rat Brain in Stereotaxic Coordinates 2007 Elsevier London
32. P.E. Phillips, G.D. Stuber, M.L. Heien, R.M. Wightman, and R.M. Carelli Subsecond dopamine release promotes cocaine seeking Nature 422 2003 614 618
33. M.N. Potenza, K.I. Hong, C.M. Lacadie, R.K. Fulbright, K.L. Tuit, and R. Sinha Neural correlates of stress-induced and cue-induced drug craving: influences of sex and cocaine dependence Am. J. Psychiatry 169 2012 406 414
34. R. Ranaldi, and W.L. Woolverton Self-administration of cocaine: scopolamine combinations by rhesus monkeys Psychopharmacology (Berl) 161 2002 442 448
35. T. Rasmussen, P. Sauerberg, E.B. Nielsen, M.D. Swedberg, C. Thomsen, M.J. Sheardown, L. Jeppesen, D.O. Calligaro, N.W. DeLapp, C. Whitesitt, J.S. Ward, H.E. Shannon, F.P. Bymaster, and A. Fink-Jensen Muscarinic receptor agonists decrease cocaine self-administration rates in drug-naive mice Eur. J. Pharmacol. 402 2000 241 246
36. M.S. Reid, J.D. Mickalian, K.L. Delucchi, and S.P. Berger A nicotine antagonist, mecamylamine, reduces cue-induced cocaine craving in cocaine-dependent subjects Neuropsychopharmacology 20 1999 297 307
37. M.S. Reid, J.D. Mickalian, K.L. Delucchi, S.M. Hall, and S.P. Berger An acute dose of nicotine enhances cue-induced cocaine craving Drug Alcohol Depend. 49 1998 95 104
38. S.J. Robbins, R.N. Ehrman, A.R. Childress, and C.P. O'Brien Using cue reactivity to screen medications for cocaine abuse: a test of amantadine hydrochloride Addict. Behav. 17 1992 491 499
39. D.J. Rohsenow, R.S. Niaura, A.R. Childress, D.B. Abrams, and P.M. Monti Cue reactivity in addictive behaviors: theoretical and treatment implications Int. J. Addict. 25 1990 957 993
40. W. Schultz Behavioral dopamine signals Trends Neurosci. 30 2007 203 210
41. R.E. See, P.J. Kruzich, and J.W. Grimm Dopamine, but not glutamate, receptor blockade in the basolateral amygdala attenuates conditioned reward in a rat model of relapse to cocaine-seeking behavior Psychopharmacology (Berl) 154 2001 301 310
42. Y. Shaham, and B.T. Hope The role of neuroadaptations in relapse to drug seeking Nat. Neurosci. 8 2005 1437 1439
43. Y. Shaham, U. Shalev, L. Lu, H. De Wit, and J. Stewart The reinstatement model of drug relapse: history, methodology and major findings Psychopharmacology (Berl) 168 2003 3 20
44. L.A. Sombers, M. Beyene, R.M. Carelli, and R.M. Wightman Synaptic overflow of dopamine in the nucleus accumbens arises from neuronal activity in the ventral tegmental area J. Neurosci. 29 2009 1735 1742
45. G.D. Stuber, F.W. Hopf, K.M. Tye, B.T. Chen, and A. Bonci Neuroplastic alterations in the limbic system following cocaine or alcohol exposure Curr. Top. Behav. Neurosci. 3 2010 3 27
46. G.D. Stuber, R.M. Wightman, and R.M. Carelli Extinction of cocaine self-administration reveals functionally and temporally distinct dopaminergic signals in the nucleus accumbens Neuron 46 2005 661 669
47. M.F. Suaud-Chagny, K. Chergui, G. Chouvet, and F. Gonon Relationship between dopamine release in the rat nucleus accumbens and the discharge activity of dopaminergic neurons during local in vivo application of amino acids in the ventral tegmental area Neuroscience 49 1992 63 72
48. M.A. Ungless, J.L. Whistler, R.C. Malenka, and A. Bonci Single cocaine exposure in vivo induces long-term potentiation in dopamine neurons Nature 411 2001 583 587
49. N.D. Volkow, J.S. Fowler, G.J. Wang, F. Telang, J. Logan, M. Jayne, Y. Ma, K. Pradhan, C. Wong, and J.M. Swanson Cognitive control of drug craving inhibits brain reward regions in cocaine abusers Neuroimage 49 2010 2536 2543
50. N.D. Volkow, G.J. Wang, F. Telang, J.S. Fowler, J. Logan, A.R. Childress, M. Jayne, Y. Ma, and C. Wong Cocaine cues and dopamine in dorsal striatum: mechanism of craving in cocaine addiction J. Neurosci. 26 2006 6583 6588
51. N.D. Volkow, G.J. Wang, D. Tomasi, F. Telang, J.S. Fowler, K. Pradhan, M. Jayne, J. Logan, R.Z. Goldstein, N. Alia-Klein, and C. Wong Methylphenidate attenuates limbic brain inhibition after cocaine-cues exposure in cocaine abusers PLoS One 5 2010 e11509
52. G.J. Wang, N.D. Volkow, J.S. Fowler, P. Cervany, R.J. Hitzemann, N.R. Pappas, C.T. Wong, and C. Felder Regional brain metabolic activation during craving elicited by recall of previous drug experiences Life Sci. 64 1999 775 784
53. F. Weiss, C.S. Maldonado-Vlaar, L.H. Parsons, T.M. Kerr, D.L. Smith, and O. Ben-Shahar Control of cocaine-seeking behavior by drug-associated stimuli in rats: effects on recovery of extinguished operant-responding and extracellular dopamine levels in amygdala and nucleus accumbens Proc. Natl. Acad. Sci. U. S. A. 97 2000 4321 4326
54. R. Wickham, W. Solecki, L.R. Rathbun, J.M. McIntosh, and N.A. Addy Ventral tegmental area α6β2 nicotinic acetylcholine receptors modulate phasic dopamine release in the nucleus accumbens core Psychopharmacology 2013 April 30 (in press) [Epub ahead of print]
55. J. Yeomans, and M. Baptista Both nicotinic and muscarinic receptors in ventral tegmental area contribute to brain-stimulation reward Pharmacol. Biochem. Behav. 57 1997 915 921
56. I.A. Yun, K.T. Wakabayashi, H.L. Fields, and S.M. Nicola The ventral tegmental area is required for the behavioral and nucleus accumbens neuronal firing responses to incentive cues J. Neurosci. 24 2004 2923 2933
57. V. Zachariou, B.J. Caldarone, A. Weathers-Lowin, T.P. George, J.D. Elsworth, R.H. Roth, J.P. Changeux, and M.R. Picciotto Nicotine receptor inactivation decreases sensitivity to cocaine Neuropsychopharmacology 24 2001 576 589
58. L. Zanetti, A. de Kerchove D'Exaerde, A. Zanardi, J.P. Changeux, M.R. Picciotto, and M. Zoli Inhibition of both alpha7* and beta2* nicotinic acetylcholine receptors is necessary to prevent development of sensitization to cocaine-elicited increases in extracellular dopamine levels in the ventral striatum Psychopharmacology (Berl) 187 2006 181 188
59. L. Zanetti, M.R. Picciotto, and M. Zoli Differential effects of nicotinic antagonists perfused into the nucleus accumbens or the ventral tegmental area on cocaine-induced dopamine release in the nucleus accumbens of mice Psychopharmacology (Berl) 190 2007 189 199
60. W. Zhou, H. Liu, F. Zhang, S. Tang, H. Zhu, M. Lai, and P.W. Kalivas Role of acetylcholine transmission in nucleus accumbens and ventral tegmental area in heroin-seeking induced by conditioned cues Neuroscience 144 2007 1209 1218
61. L.S. Zweifel, J.P. Fadok, E. Argilli, M.G. Garelick, G.L. Jones, T.M. Dickerson, J.M. Allen, S.J. Mizumori, A. Bonci, and R.D. Palmiter Activation of dopamine neurons is critical for aversive conditioning and prevention of generalized anxiety Nat. Neurosci. 14 2011 620 626
62. L.S. Zweifel, J.G. Parker, C.J. Lobb, A. Rainwater, V.Z. Wall, J.P. Fadok, M. Darvas, M.J. Kim, S.J. Mizumori, C.A. Paladini, P.E. Phillips, and R.D. Palmiter Disruption of NMDAR-dependent burst firing by dopamine neurons provides selective assessment of phasic dopamine-dependent behavior Proc. Natl. Acad. Sci. U. S. A. 106 2009 7281 7288