Both nicotinic and muscarinic receptors in ventral tegmental area contribute to brain-stimulation reward

Pharmacology Biochemistry and Behavior

Volumn 57, Issue 4, 1997, Pages 915-921

  Yeomans, John ^a   Baptista, Marco ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

Atropine; Cholinergic; Dohydro erythroidine; Dopamine; Mecamylamine; Mesopontine; Pedunculopontine; Self stimulation

Indexed keywords

ATROPINE; DIHYDRO BETA ERYTHROIDINE; MECAMYLAMINE; MUSCARINIC RECEPTOR; NICOTINE; NICOTINIC RECEPTOR;

ANIMAL EXPERIMENT; ARTICLE; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; MALE; MEDIAL FOREBRAIN BUNDLE; NERVE CELL STIMULATION; NONHUMAN; PRIORITY JOURNAL; RAT; SMOKING; VENTRAL TEGMENTUM;

ANIMALS; ATROPINE; DIHYDRO-BETA-ERYTHROIDINE; MALE; MECAMYLAMINE; MICROINJECTIONS; NICOTINE; NICOTINIC AGONISTS; NICOTINIC ANTAGONISTS; RATS; RATS, WISTAR; RECEPTORS, MUSCARINIC; RECEPTORS, NICOTINIC; REWARD; SELF STIMULATION; VENTRAL TEGMENTAL AREA;

ANIMALIA; NICOTIANA TABACUM;

EID: 0030847966     PISSN: 00913057     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0091-3057(96)00467-4     Document Type: Article

References (56)

1. Bauco, P.; Wise, R. A.: Potentiation of lateral hypothalamic and midline mesencephalic brain stimulation reinforcement by nicotine: Examination of repeated treatment. J. Pharmacol. Exp. Ther. 272:294-301; 1994.
2. Blaha, C. D.; Allen, L. F.; Das, S.; Inglis, W. L.; Latimer, M. P.; Vincent, S. R.; Winn, P.: Modulation of dopamine efflux in the nucleus accumbens after cholinergic stimulation of the ventral tegmental area in intact, pedunculopantine tegmental nucleuslesioned and laterodorsal tegmental nucleus-lesioned rats. J. Neurosci. 16:714-722; 1996.
3. Blaha, C. D.; Winn, P.: 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; 1993.
4. Bolam, J. P.; Francis, C. M.; Henderson, Z.: Cholinergic input to dopaminergic neurons in the substantia nigra: A double immunocytochemical study. Neuroscience 41:483-494; 1991.
5. Calabresi, P.; Lacey, M. G.; North, R. A.: Nicotinic excitation of rat ventral tegmental neurons in vitro studied by intracellular recording. Br. J. Pharmacol. 98:135-140; 1989.
6. Campbell, K. A.; Evans, G.; Gallistel, C. R.: A microcomputer-based method for physiologically interpretable measurement of the rewarding efficacy of brain stimulation. Physiol. Behav. 35: 395-403; 1985.
7. Clarke, P. B. S.: Mesolimbic dopamine activation - The key to nicotine reinforcement? In: Bock, G. and Marsh, J., eds. The biology of nicotine dependence. Chichester, UK: Wiley; 1990:153-168.
8. Clarke, P. B. S.; Fu, D. S.; Jakubovic, A.; Fibiger, H. C.: Evidence that mesolimbic dopaminergic activation underlies the locomotor stimulant actions of nicotine in rats. J. Pharmacol. Exp. Ther. 246:701-708; 1988.
9. Clarke, P. B. S.; Hommer, D. W.; Pert, A.; Skirboll, L. R.: Innervation of substantia nigra neurons by cholinergic afferents from pedunculopontine nucleus in the rat: Neuroanatomical and electrophysiological evidence. Neuroscience 23:1011-1019; 1988.
10. Clarke, P. B. S.; Kumar, R.: Effects of nicotine and amphetamine on intracranial self-stimulation in a shuttle box in rats. Psychopharmacology 84:109-114; 1983.
11. Clarke, P. B. S.; Pert, A.: Autoradiographic evidence for nicotine receptors on nigrostriatal and mesolimbic neurons. Brain Res. 348: 355-358; 1985.
12. Corrigall, W. A.; Coen, K. M.: Nicotine maintains robust self-administration in rats on a limited access schedule. Psychopharmacology 104:473-478; 1989.
13. Corrigall, W. A.; Coen, K. M.; Adamson, K. L.: Self-administered nicotine activates the mesolimbic dopamine system through the ventral tegmental area. Brain Res. 653:278-284; 1994.
14. Corrigall, W. A.; Franklin, K. B. J.; Coen, K. M.; Clarke, P. B. S.: The mesolimbic dopaminergic system is implicated in the reinforcing effects of nicotine. Psychopharmacology 107:285-289; 1992.
15. Druhan, J.; Fibiger, H. C.; Phillips, A. G.: Differential effects of cholinergic drugs on discriminative cues and self-stimulation produced by electrical stimulation of the ventral tegmental area. Psychopharmacology 97:331-338; 1989.
16. Edmonds, D. E.; Gallistel, C. R.: Reward versus performance in self-stimulation: Electrode specific effects of α-methyl-p-tyrosine on reward in the rat. J. Comp. Physiol. Psychol. 91:962-974; 1977.
17. Fujimoto, K.; Ikeguchi, K.; Yoshida, M.: Decrease and recovery of choline acetyltransferase activity in medial thalamus and ventral tegmental area after destruction of pedunculopontine areas in the rat. Neurosci. Res. 9:48-53; 1990.
18. Futami, T.; Kitai, S. T.; Takakusaki, E.: Glutamatergic and cholinergic inputs from the pedunculopontine tegmental nucleus to dopamine neurons in the substantia nigra pars compacta. Neurosci. Res. 21:331-342; 1995.
19. Gould, E.; Woolf, N. J.; Butcher, L. L.: Cholinergic projections to the substantia nigra from the pedunculopontine and laterodorsal tegmental nuclei. Neuroscience 28:611-623; 1989.
20. Hernandez-Lopez, S.; Gongora-Alfaro, J. L.; Martinez-Fong, D.; Aceves, J. A.: Cholinergic input to the substantia nigra pars compacta increases striatal dopamine metabolism measured by in vivo voltammetry. Brain Res. 598:114-120; 1992.
21. Huston-Lyons, D.; Kornetzky, C.: Effects of nicotine on the threshold for rewarding brain stimulation in rats. Pharmacol. Biochem. Behav. 41:755-759; 1992.
22. Imperato, A.; Mulas, A.; Di Chiara, G.: Nicotine preferentially stimulates dopamine release in the limbic system of freely moving rats. Eur. J. Pharmacol. 132:337-338; 1986.
23. Kayama, Y.; Ogawa, T.: Electrophysiology of ascending, possibly cholinergic neurons in the rat laterodorsal tegmental nucleus: Comparison with monoamine neurons. Neurosci. Lett. 77:277-282; 1987.
24. Kofman, O.; McGlynn, S.; Olmstead, M. C.; Yeomans, J. S.: Differential effects of atropine, procaine and dopamine in the rat ventral tegmentum on lateral hypothalamic rewarding brain stimulation. Behav. Brain Res. 38:55-68; 1990.
25. Kofman, O.; Yeomans, J. S.: Cholinergic antagonists in ventral tegmentum elevate thresholds for lateral hypothalamic and brainstem self-stimulation. Pharmacol. Biochem. Behav. 31:547-559; 1989.
26. Kraus, V. A.; Lapina, L: Effect of direct electrical and chemical stimulation on the excitability of the hypothalamic nuclei and the self-stimulation reaction in dogs. Zh. Vyssh. Nervn. Deyat. Im. I. P. Pavlova 22:1226-1232; 1972.
27. Lacey, M. G.; Calabresi, P.; North, R. A.: Muscarine depolarizes substantia nigra zona compacta and ventral tegmental neurons in vitro through M1-like receptors. J. Pharmacol. Exp. Ther. 253: 395-400; 1991.
28. Latiff, A. A.; Smith, L. A.; Lang, W. J.: Effects of changing dosage and urinary pH in rats self-administering nicotine on a food delivery schedule. Pharmacol. Biochem. Behav. 13:209-213; 1980.
29. Mathur, A.; Yeomans, J. S.: Locomotion and stereotypy induced by microinjections of scopolamine into the pedunculopontine nucleus: Involvement of dopamine cells. Soc. Neurosci. Abstr. 19:758; 1993.
30. McGehee, D. S.; Heath, M. J. S.; Gelber, S.; Devay, P.; Role, L. W.: Nicotine enhancement of fast excitatory synaptic transmission in CNS by presynaptic receptors. Science 269:1692-1696; 1995.
31. Murray, B.; Shizgal, P.: Behavioral measures of conduction velocity and refractory period for reward-relevant axons in the anterior LH and VTA. Physiol. Behav. 59:643-652; 1996.
32. Museo, E.; Wise, R. A.: Locomotion induced by ventral tegmental microinjections of a nicotinic agonist. Pharmacol. Biochem. Behav. 35:735-737; 1990.
33. Niijima, K.; Yoshida, M.: Activation of mesencephalic dopamine neurons by chemical stimulation of the nucleus tegmenti pedunculopontinus pars compacta. Brain Res. 451:163-171; 1988.
34. Nisell, M.; Nomikos, G. G.; Svensson, T. H.: Systemic nicotine induced dopamine release in the rat nucleus accumbens is regulated by nicotinic receptors in the ventral tegmental area. Synapse 16:36-44; 1994.
35. Paxinos, G.; Watson, C.: The rat brain in stereotaxic coordinates, 2nd ed. Sydney: Academic Press; 1986.
36. Reavill, C.; Stolerman, I. P.: Locomotor activity in rats after administration of nicotinic agonists intracerebrally. Br. J. Pharmacol. 99:273-278; 1990.
37. Redgrave, P.; Horrell, R. I.: Potentiation of central reward by localized perfusion of acetylcholine and 5-hydroxytryptamine. Nature 262:305-307; 1976.
38. Semba, K.; Fibiger, H. C.: Afferent connections of the laterodorsal and the pedunculopontine tegmental nuclei in the rat: A retro- and antero-grade transport and immunohistochemical study. J. Comp. Neurol. 323:387-410; 1992.
39. Shizgal, P.; Bielajew, C.; Corbett, D.; Skelton, R.; Yeomans, J. S.: Collision-like effect from concurrent electrical stimulation of two rewarding sites of the brain. J. Comp. Physiol. Psychol. 94:227-237; 1980.
40. Steininger, T. L.; Rye, D. B.; Wainer, B. H.: Afferent projections to the cholinergic pedunculopontine nucleus and adjacent midbrain extrapyramidal area in the albino rat. I. Retrograde tracing studies. J. Comp. Neurol. 321:515-543; 1992.
41. Stellar, J. R.; Corbett, D.: Regional neuroleptic microinjections indicate a role for nucleus accumbens in lateral hypothalamic self-stimulation reward. Brain Res. 477:126-143; 1989.
42. Vilaro, M. T.; Palacios, J. M.; Mengod, G.: Localization of m5 muscarinic receptor mRNA in rat brain examined by in situ hybridization histochemistry. Neurosci. Lett. 114:154-159; 1990.
43. Wada, E.; Wada, K.; Boulter, J.; Deneris, E.; Heinemann, S.; Patrick J.; Swanson, L. W.: Distribution of α2, α3, α4, and β2 neuronal nicotinic receptor subunit mRNAs in the central nervous system: A hybridization study in the rat. J. Comp. Neurol. 284: 314-335; 1989.
44. Weiner, D. M.; Levey, A. I.; Brann, M. R.: Expression of muscarinic acetylcholine and dopamine receptor mRNAs in rat basal ganglia. Proc. Natl. Acad. Sci. USA 87:7050-7054; 1990.
45. Williams, M.; Robinson, J. L.: Binding of the nicotinic cholinergic antagonist dihydro-beta-erythroidine, to rat brain tissue. J. Neurosci. 4:2906-2911; 1984.
46. Wise, R. A.; Rompre, P.-P.: Brain dopamine and reward. Annu. Rev. Psychol. 40:191-225; 1989.
47. Yeomans, J. S.: Quantitative measurement of neural post-stimulation excitability with behavioral methods. Physiol. Behav. 15: 593-602; 1975.
48. Yeomans, J. S.: Absolute refractory periods of self-stimulation neurons. Physiol. Behav. 22:911-919; 1979.
49. Yeomans, J. S.: Mechanisms of brain-stimulation reward. In: Epstein, A. N.; Morrison, A. R., eds. Progress in psychobiology and physiological psychology, vol. 13. New York: Academic Press; 1988:227-266.
50. Yeomans, J. S.: Principles of brain stimulation. New York: Oxford University Press; 1990.
51. Yeomans, J. S.: Role of tegmental cholinergic neurons in dopaminergic activation, antimuscarinic psychosis and schizophrenia. Neuropsychopharmacology 12:3-16; 1995.
52. Yeomans, J. S.; Baptista, M.; Takeuchi, J.; Kofman, O.; Ralph, M. R.: The role of nicotinic and muscarinic receptors in the ventral tegmental area in intracranial self-stimulation. Soc. Neurosci. Abstr. 21:732; 1995.
53. Yeomans, J. S.; Kofman, O.; McFarlane, V.: Cholinergic involvement in lateral hypothalamic rewarding brain stimulation. Brain Res. 329:19-26; 1985.
54. Yeomans, J. S.; Maidment, N. S.; Bunney, B. S.: Excitability properties of medial forebrain bundle axons of A9 and A10 dopamine cells. Brain Res. 450:86-93; 1988.
55. Yeomans, J. S.; Mathur, A.; Tampakeras, M.: Rewarding brain stimulation: Role of tegmental cholinergic neurons that activate dopamine neurons. Behav. Neurosci. 107:1077-1087; 1993.
56. Yeomans, J. S.; Mercouris, N.; Ellard, C.: Behaviorally measured refractory periods are lengthened by reducing electrode tip exposure or raising current. Behav. Neurosci. 99:913-928; 1985.