M 5 muscarinic receptors mediate striatal dopamine activation by ventral tegmental morphine and pedunculopontine stimulation in mice

PLoS ONE

Volumn 6, Issue 11, 2011, Pages

  Steidl, Stephan ^a   Miller, Anthony D ^b   Blaha, Charles D ^b   Yeomans, John S ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b University of Memphis

Author keywords

[No Author keywords available]

Indexed keywords

DOPAMINE; MORPHINE; MUSCARINIC M5 RECEPTOR; SCOPOLAMINE; URETHAN;

AMPEROMETRY; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEPTH STIMULATION; CATECHOLAMINE RELEASE; CATECHOLAMINE UPTAKE; CONTROLLED STUDY; ELECTROSTIMULATION; FOREBRAIN; KNOCKOUT MOUSE; MALE; MOUSE; NEOSTRIATUM; NONHUMAN; NUCLEUS ACCUMBENS; PEDUNCULOPONTINE TEGMENTAL NUCLEUS; VENTRAL TEGMENTUM; WILD TYPE; ANIMAL; BASAL GANGLION; METABOLISM; MOUSE MUTANT; PHYSIOLOGY;

MUS;

ANIMALS; BASAL GANGLIA; DOPAMINE; ELECTRIC STIMULATION; MALE; MICE; MICE, KNOCKOUT; MORPHINE; PEDUNCULOPONTINE TEGMENTAL NUCLEUS; RECEPTOR, MUSCARINIC M5; VENTRAL TEGMENTAL AREA;

EID: 81055140948     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0027538     Document Type: Article

References (38)

1. Wise RA, (2002) Brain reward circuitry: insights from unsensed incentives. Neuron 36: 229-240.
2. Johnson SW, North RA, (1992) Opioids excite dopamine neurons by hyperpolarization of local interneurons. J Neurosci 12: 483-488.
3. Gysling K, Wang RY, (1983) Morphine-induced activation of A10 dopamine neurons in the rat. Brain Res 277: 119-127.
4. Matthews RT, German DC, (1984) Electrophysiological evidence for excitation of rat ventral tegmental area dopamine neurons by morphine. Neuroscience 11: 617-625.
5. Leone P, Pocock D, Wise RA, (1991) Morphine-dopamine interaction: ventral tegmental morphine increases nucleus accumbens dopamine release. Pharmacol Biochem Behav 39: 469-472.
6. Spanagel R, Herz A, Shippenberg TS, (1992) Opposing tonically active endogenous opioid systems modulate the mesolimbic dopaminergic pathway. Proc Natl Acad Sci USA 89: 2046-2050.
7. Oakman SA, Faris PL, Kerr PE, Cozzari C, Hartman BK, (1995) Distribution of pontomesencephalic cholinergic neurons projecting to substantia nigra differs significantly from those projecting to ventral tegmental area. J Neurosci 15: 5859-5869.
8. Blaha CD, Allan LF, Das S, Inglis WL, Latimer MP, et al. (1996) 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: 714-722.
9. Forster GL, Falcon AJ, Miller AD, Heruc GA, Blaha CD, (2002) Effects of laterodorsal tegmentum excitotoxic lesions on behavioral and dopamine responses evoked by morphine and d-amphetamine. Neuroscience 114: 817-823.
10. Miller AD, Forster GL, Metcalf KM, Blaha CD, (2002) Excitotoxic lesions of the pedunculopontine differentially mediate morphine- and d-amphetamine-evoked striatal dopamine efflux and behaviors. Neuroscience 111: 351-362.
11. Miller AD, Forster GL, Yeomans JS, Blaha CD, (2005) Midbrain muscarinic receptors modulate morphine-induced accumbal and striatal dopamine efflux in the rat. Neuroscience 136: 531-538.
12. Bechara A, Harrington F, Nader K, van der Kooy D, (1992) Neurobiology of motivation: Double dissociation of two motivational mechanisms mediating opiate reward in drug-naive versus drug-dependent animals. Behav Neurosci 106: 798-807 Eur J Neurosci 21:1837-1846.
13. Olmstead MC, Munn EM, Franklin KBJ, Wise RA, (1998) Effects of pedunculopontine tegmental nucleus lesions on responding for intravenous heroin under different schedules of reinforcement. J Neurosci 18: 5035-5044.
14. Rezayof A, Nazari-Serenjeh F, Zarrindast MR, Sepehri H, Delphi L, (2007) Morphine-induced place preference: Involvement of cholinergic receptors of the ventral tegmental area. Eur J Pharmacol 562: 92-102.
15. Vilaro MT, Palacios JM, Mengod G, (1990) Localization of M5 muscarinic receptor mRNA in rat brain examined by in situ hybridization histochemistry. Neurosci Lett 114: 154-159.
16. Weiner DM, Levey AI, Brann MR, (1990) Expression of muscarinic acetylcholine and dopamine receptor mRNAs in rat basal ganglia. Proc Natl Acad Sci USA 87: 7050-7054.
17. Forster GL, Blaha CD, (2000) Laterodorsal tegmental stimulation elicits dopamine efflux in the rat nucleus accumbens by activation of acetylcholine and glutamate receptors in the ventral tegmental area. Eur J Neurosci 12: 3596-3604.
18. Forster GL, Blaha CD, (2003) Pedunculopontine tegmental stimulation evokes striatal dopamine efflux by activation of acetylcholine and glutamate receptors in the midbrain and pons of the rat. Eur J Neurosci 17: 751-762.
19. Forster GL, Yeomans JS, Takeuchi J, Blaha CD, (2001) M5 muscarinic receptors are required for prolonged accumbal dopamine release after electrical stimulation of the pons in mice. J Neurosci 22: RC190.
20. Basile AS, Fedorova I, Zapata A, Liu X, Shippenberg T, et al. (2002) Deletion of the M5 muscarinic acetylcholine receptor attenuates morphine reinforcement and withdrawal but not morphine analgesia. Proc Natl Acad Sci USA 99: 11452-11457.
21. Steidl S, Yeomans JS, (2008) M5 muscarinic receptor knockout mice show reduced morphine-induced locomotion, but increased locomotion following cholinergic antagonism in the ventral tegmental area. J Pharmacol Exp Ther 328: 1-13.
22. Takakusaki K, Shiroyama T, Kitai ST, (1997) Two types of cholinergic neurons in the rat tegmental peduculopontine nucleus: electrophysiological and morphological characterization. Neuroscience 79: 1089-1109.
23. Yeomans JS, Maidment NT, Bunney BS, (1988) Excitability properties of medial forebrain bundle axons of A9 and A10 dopamine cells. Brain Res 450: 86-93.
24. Ferrari-DiLeo G, Waelbroeck M, Mash DC, Flynn DD, (1994) Selective labeling and localization of the M4 (m4) muscarinic receptor subtype. Mol Pharmacol 46: 1028-1035.
25. Takeuchi J, Fulton J, Jia ZP, Abramov-Newerly W, Jamot L, et al. (2002) Increased drinking in mutant mice with truncated M5 muscarinic receptor genes. Pharmacol Biochem Behav 72: 117-123.
26. Blaha CD, Winn P, (1993) Modulation of dopamine efflux in the striatum following cholinergic stimulation of the substantia nigra in intact and pedunculopontine tegmental nucleus-lesioned rats. J Neurosci 13: 1035-1044.
27. Miller AD, Blaha CD, (2005) Midbrain muscarinic receptor mechanisms underlying regulation of mesoaccumbens and nigrostriatal dopaminergic transmission in the rat.
28. Narita M, Nagumo Y, Hashimoto S, Narita M, Khotib J, et al. (2006) Direct involvement of orexinergic systems in the activation of the mesolimbic dopamine pathway and related behaviors induced by morphine. J Neurosci 26: 398-405.
29. David V, Cazala P, (1994) A comparative study of self-administration of morphine into the amygdala and the ventral tegmental area in mice. Behav Brain Res 65: 205-211.
30. Laviolette SR, Gallegos RA, Henriksen SJ, van der Kooy D, (2004) Opiate state controls bi-directional reward signaling via GABAA receptors in the ventral tegmental area. Nat Neurosci 7: 160-169.
31. Kohlmeier KA, Kristiansen U, (2010) GABAergic actions on cholinergic laterodorsal tegmental neurons: implications for control of behavioral state. Neurosci 171: 812-829.
32. 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 the substantia nigra compacta. J Comp Neurol 513: 566-596.
33. Lecca S, Melis M, Luchicchi A, Ennas MG, Castelli MP, et al. (2011) Effects of drugs of abuse on putative rostromedial tegmental neurons, inhibitory afferents to midbrain dopamine cells. Neuropsychopharmacology 36: 589-602.
34. Yeomans JS, Forster G, Blaha CD, (2001) M5 muscrinic receptors are needed for slow activation of dopamine neurons and for rewarding brain stimulation. Life Sci 68: 2449-2456.
35. Blaha CD, Jung ME, (1991) Electrochemical evaluation of stearate-modified graphite paste electrodes: selective detection of dopamine is maintained after exposure to brain tissue. J Electroanal Chem 310: 317-334.
36. Blaha CD, Phillips AG, (1996) A critical assessment of electrochemical procedures applied to the measurement of dopamine and its metabolites during drug-induced and species-typical behaviours. Behav Pharmacol 7: 675-708.
37. Steriade M, Datta S, Pare D, Oakson G, Curro Dossi R, (1990) Neuronal activities in brain-stem cholinergic nuclei related to tonic activation processes in thalamocortical systems. J Neurosci 10: 2541-2559.
38. Paxinos G, Franklin KBJ, (2004) The mouse brain in stereotaxic coordinates San Diego, CA Academic Press.