Cholinergic control of morphine-induced locomotion in rostromedial tegmental nucleus versus ventral tegmental area sites

European Journal of Neuroscience

Volumn 38, Issue 5, 2013, Pages 2774-2785

  Wasserman, David I ^a   Wang, Haoran G ^a   Rashid, Asim J ^b   Josselyn, Sheena A ^b   Yeomans, John S ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

Author keywords

Dopamine; GABA; Mouse; Muscarinic; Opioid

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; ACETYLCHOLINE; CHOLERA TOXIN B SUBUNIT; CHOLINESTERASE; MORPHINE; MUSCARINIC M5 RECEPTOR; SODIUM CHLORIDE; TYROSINE 3 MONOOXYGENASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; GENE EXPRESSION; GENE TRANSFER; GENETIC TRANSFECTION; HERPES SIMPLEX VIRUS; KNOCKOUT MOUSE; LOCOMOTION; M5 GENE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; RECEPTOR GENE; ROSTROMEDIAL TEGMENTAL NUCLEUS; STEREOTYPY; TEGMENTUM; VENTRAL TEGMENTUM;

EID: 84883446778     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12279     Document Type: Article

References (49)

1. Balcita-Pedicino, J.J., Omelchenko, N., Bell, R. & Sesack, S.R. (2011) The inhibitory influence of the lateral habenula on midbrain dopamine cells: ultrastructural evidence for indirect mediation via the rostromedial mesopontine tegmental nucleus. J. Comp. Neurol., 519, 1143-1164.
2. Barrot, M. & Thome, J. (2011) Discovering a new anatomical structure in the brain: implications for neuropsychiatry and therapy. World J. Biol. Psychia., 12 (Suppl 1), 19-22.
3. Barrot, M., Sesack, S.R., Georges, F., Pistis, M., Hong, S. & Jhou, T.C. (2012) Braking dopamine systems: a new GABA master structure for mesolimbic and nigrostriatal functions. J. Neurosci., 32, 14094-14101.
4. Basile, A.S., Fedorova, I., Zapata, A., Liu, X., Shippenberg, T., Duttaroy, A., Yamada, M. & Wess, J. (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.
5. Bolam, J.P., Francis, C.M. & Henderson, Z. (1991) Cholinergic input to dopaminergic neurons in the substantia nigra: a double immunocytochemical study. Neuroscience, 41, 483-494.
6. Bourdy, R. & Barrot, M. (2012) A new control center for dopaminergic systems: pulling the VTA by the tail. Trends Neurosci., 35, 681-690.
7. Carlezon, W.A., Boundy, V.A., Haile, C.N., Lane, S.B., Kalb, R.G., Neve, R.L. & Nestler, E.J. (1997) Sensitization to morphine induced by viral-mediated gene transfer. Science, 277, 812-815.
8. Conte, W.L., Kamishina, H. & Reep, R.L. (2009) Multiple neuroanatomical tract-tracing using fluorescent Alexa Fluor conjugates of cholera toxin subunit B in rats. Nat. Protoc., 4, 1157-1166.
9. Dobi, A., Margolis, E.B., Wang, H.L., Harvey, B.K. & 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. Forster, G.L. & Blaha, C.D. (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.
11. Forster, G.L., Yeomans, J.S., Takeuchi, J. & Blaha, C.D. (2001) M5 muscarinic receptors are required for prolonged accumbal dopamine release after electrical stimulation of the pons in mice. J. Neurosci. 22, RC190.
12. Forster, G.L., Falcon, A.J., Miller, A.D., Heruc, G.A. & Blaha, C.D. (2002) Effects of laterodorsal tegmentum excitotoxic lesions on behavioral and dopamine responses evoked by morphine and d-amphetamine. Neuroscience, 114, 817-823.
13. Franklin, K.B.J. & Paxinos, G. (2007) The Mouse Brain in Stereotaxic Coordinates, 3rd Edn. Academic Press, San Diego, CA.
14. Garzón, M. & Pickel, V.M. (2001) Plasmalemmal mu-opioid receptor distribution mainly in nondopaminergic neurons in the rat ventral tegmental area. Synapse, 41, 311-328.
15. Han, J.H., Kushner, S.A., Yiu, A.P., Hsiang, H.L., Buch, T., Waisman, A., Bontempi, B., Neve, R.L., Frankland, P.W. & Josselyn, S.A. (2009) Selective erasure of a fear memory. Science, 323, 1492-1496.
16. Hong, S., Jhou, T.C., Smith, M., Saleem, K.S. & 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.
17. Ikemoto, S. (2010) Brain reward circuitry beyond the mesolimbic dopamine system: a neurobiological theory. Neurosci. Biobehav. R., 35, 129-150.
18. Jalabert, M., Bourdy, R., Courtin, J., Veinante, P., Manzoni, O.J., Barrot, M. & Georges, F. (2011) Neuronal circuits underlying acute morphine action on dopamine neurons. Proc. Natl. Acad. Sci. USA, 108, 16446-16450.
19. Jhou, T.C., Fields, H.L., Baxter, M.G., Saper, C.B. & Holland, P.C. (2009a) The rostromedial tegmental nucleus (RMTg), a GABAergic afferent to midbrain dopamine neurons, encodes aversive stimuli and inhibits motor responses. Neuron, 61, 786-800.
20. Jhou, T.C., Geisler, S., Marinelli, M., Degarmo, B.A. & Zahm, D.S. (2009b) 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.
21. Jhou, T.C., Xu, S.P., Lee, M.R., Gallen, C.L. & Ikemoto, S. (2012) Mapping of reinforcing and analgesic effects of the mu opioid agonist Endomorphin-1 in the ventral midbrain of the rat. Psychopharmacology, 224, 303-312.
22. Johnson, S.W. & North, R.A. (1992) Opioids excite dopamine neurons by hyperpolarization of local interneurons. J. Neurosci., 12, 483-488.
23. Kalivas, P.W., Widerlöv, E., Stanley, D., Breese, G. & Prange, A.J. Jr. (1983) Enkephalin action on the mesolimbic system: a dopamine-dependent and a dopamine-independent increase in locomotor activity. J. Pharmacol. Exp. Ther., 227, 229-237.
24. Lavezzi, H.N. & Zahm, D.S. (2011) The mesopontine rostromedial tegmental nucleus: an integrative modulator of the reward system. Basal Ganglia, 1, 191-200.
25. Lavezzi, H.N., Parsley, K.P. & Zahm, D.S. (2012) Mesopontine rostromedial tegmental nucleus neurons projecting to the dorsal raphe and pedunculopontine tegmental nucleus: psychostimulant-elicited Fos expression and collateralization. Brain Struct. Funct., 217, 719-734.
26. A receptors signal bidirectional reward transmission from the ventral tegmental area to the tegmental pedunculopontine nucleus as a function of opiate state. Eur. J. Neurosci., 20, 2179-2187.
27. Lecca, S., Melis, M., Luchicchi, A., Ennas, M.G., Castelli, M.P., Muntoni, A.L. & Pistis, M. (2011) Effects of drugs of abuse on putative rostromedial tegmental neurons, inhibitory afferents to midbrain dopamine cells. Neuropsychopharmacol., 36, 589-602.
28. Lecca, S., Melis, M., Luchicchi, A., Muntoni, A.L. & Pistis, M. (2012) Inhibitory inputs from rostromedial tegmental neurons regulate spontaneous activity of midbrain dopamine cells and their responses to drugs of abuse. Neuropsychopharmacol., 37, 1164-1176.
29. Lepore, M. & Franklin, K.B. (1996) N-methyl-D-aspartate lesions of the pedunculopontine nucleus block acquisition and impair maintenance of responding reinforced with brain stimulation. Neuroscience, 71, 147-155.
30. Liu, M., Thankachan, S., Kaur, S., Begum, S., Blanco-Centurion, C., Sakurai, T., Yanagisawa, M., Neve, R. & Shiromani, P.J. (2008) Orexin (hypocretin) gene transfer diminishes narcoleptic sleep behavior in mice. Eur. J. Neurosci., 28, 1382-1393.
31. Matsui, A. & Williams, J.T. (2011) Opioid-sensitive GABA inputs from rostromedial tegmental nucleus synapse onto midbrain dopamine neurons. J. Neurosci., 31, 17729-17735.
32. Miller, A.D., Forster, G.L., Metcalf, K.M. & Blaha, C.D. (2002) Excitotoxic lesions of the pedunculopontine differentially mediate morphine- and d-amphetamine-evoked striatal dopamine efflux and behaviors. Neuroscience, 111, 351-362.
33. Miller, A.D., Forster, G.L., Yeomans, J.S. & Blaha, C.D. (2005) Midbrain muscarinic receptors modulate morphine-induced accumbal and striatal dopamine efflux in the rat. Neuroscience, 136, 531-538.
34. Neve, R.L. & Geller, A.I. (1996) A defective herpes simplex virus vector system for gene delivery into the brain: comparison with alternative gene delivery systems and usefulness for gene therapy. Clin. Neurosci., 3, 262-267.
35. Oakman, S.A., Faris, P.L., Kerr, P.E., Cozzari, C. & Hartman, B.K. (1995) Distribution of pontomesencephalic cholinergic neurons projecting to substantia nigra differs significantly from those projecting to ventral tegmental area. J. Neurosci., 15, 5859-5869.
36. Olmstead, M.C., Munn, E.M., Franklin, K.B. & Wise, R.A. (1998) Effects of pedunculopontine tegmental nucleus lesions on responding for intravenous heroin under different schedules of reinforcement. J. Neurosci., 18, 5035-5044.
37. Omelchenko, N. & Sesack, S.R. (2006) Cholinergic axons in the rat ventral tegmental area synapse preferentially onto mesoaccumbens dopamine neurons. J. Comp. Neurol., 494, 863-875.
38. Reever, C.M., Ferrari-DiLeo, G. & Flynn, D.D. (1997) The M5 (m5) receptor subtype: fact or fiction? Life Sci., 60, 1105-1112.
39. Steidl, S. & Yeomans, J.S. (2009) M5 muscarinic receptor knockout mice show reduced morphine-induced locomotion but increased locomotion after cholinergic antagonism in the ventral tegmental area. J. Pharmacol. Exp. Ther., 328, 263-275.
40. Steidl, S., Miller, A.D., Blaha, C.D. & Yeomans, J.S. (2011) M5 muscarinic receptors mediate striatal dopamine activation by ventral tegmental morphine and pedunculopontine stimulation in mice. PLoS ONE, 6, e27538.
41. Taniguchi, H., He, M., Wu, P., Kim, S., Paik, R., Sugino, K., Kvitsiani, D., Fu, Y., Lu, J., Lin, Y., Miyoshi, G., Shima, Y., Fishell, G., Nelson, S.B. & Huang, Z.J. (2011) A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex. Neuron, 71, 995-1013.
42. Tzschentke, T.M. (2001) Pharmacology and behavioral pharmacology of the mesocortical dopamine system. Prog. Neurobiol., 63, 241-320.
43. Vertes, R.P. (1991) A PHA-L analysis of ascending projections of the dorsal raphe nucleus in the rat. J. Comp. Neurol., 313, 643-668.
44. Vilaro, M.T., Palacios, J.M. & Mengod, G. (1990) Localization of M5 muscarinic receptor mRNA in rat brain examined by in situ hybridization histochemistry. Neurosci. Lett., 114, 154-159.
45. Wang, H.-L. & Morales, M. (2009) Pedunculopontine and laterodorsal tegmental nuclei contain distinct populations of cholinergic, glutamatergic and GABAergic neurons in the rat. Eur. J. Neurosci., 29, 340-358.
46. Watabe-Uchida, M., Zhu, L., Ogawa, S.K., Vamanrao, A. & Uchida, N. (2012) Whole-brain mapping of direct inputs to midbrain dopamine neurons. Neuron, 74, 858-873.
47. Weiner, D.M., Levey, A.I. & Brann, M.R. (1990) Expression of muscarinic acetylcholine and dopamine receptor mRNAs in rat basal ganglia. Proc. Natl. Acad. Sci. USA, 87, 7050-7054.
48. Westerink, B.H., Kwint, H.F. & De Vries, J.B. (1996) The pharmacology of mesolimbic dopamine neurons: a dual-probe microdialysis study in the ventral tegmental area and nucleus accumbens of the rat brain. J. Neurosci., 16, 2605-2611.
49. Yeomans, J.S. (2012) Muscarinic receptors in brain stem and mesopontine cholinergic arousal functions. Handb. Exp. Pharmacol., 208, 243-259.