Differential effects of nicotine on the activity of substantia nigra and ventral tegmental area dopaminergic neurons in vitro

Acta Neurobiologiae Experimentalis

Volumn 64, Issue 2, 2004, Pages 119-130

  Teo, Min Yau ^a   Van Wyk, Michiel ^a   Lin, John ^a   Lipski, Janusz ^a  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

Extracellular recording; Nicotinic receptors; Retrograde labeling; Substantia nigra pars compacta; Ventral tegmental area

Indexed keywords

CALCIUM ION; GLUTAMATE RECEPTOR; GLUTAMATE RECEPTOR ANTAGONIST; GLUTAMIC ACID; MAGNESIUM ION; NICOTINE; NICOTINIC RECEPTOR;

ANIMAL TISSUE; ARTICLE; DOPAMINE RELEASE; DOPAMINERGIC NERVE CELL; IN VITRO STUDY; MESENCEPHALON; NERVE CONDUCTION; NERVE STIMULATION; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRESYNAPTIC POTENTIAL; RAT; SMOKING; SUBSTANTIA NIGRA; VENTRAL TEGMENTUM;

ANIMALS; DOPAMINE; NEURONS; NICOTINE; NICOTINIC AGONISTS; RATS; RATS, WISTAR; SUBSTANTIA NIGRA; VENTRAL TEGMENTAL AREA;

EID: 2442632825     PISSN: 00651400     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (55)

1. Arroyo-Jimenez MM, Bourgeois JP, Marubio LM, Le Sourd AM, Ottersen OP, Rinvik E, Fairen A, Changeux JP (1999) Ultrastructural localization of the alpha4-subunit of the neuronal acetylcholine nicotinic receptor in the rat substantia nigra. J Neurosci 19: 6475-6487.
2. 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.
3. Blaha CD, Allen LF, Das S, Inglis WL, Latimer MP, Vincent SR, Winn P (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.
4. Bolam JP, Francis CM, Henderson Z (1991) Cholinergic input to dopaminergic neurons in the substantia nigra: a double immunocytochemical study. Neuroscience 41: 483-494.
5. Butcher LL, Marchand R (1978) Dopamine neurons in pars compacta of the substantia nigra contain acetylcholinesterase: histochemical correlations on the same brain section. Eur J Pharmacol 52: 415-417.
6. Calabresi P, Lacey MG, North RA (1989) Nicotinic excitation of rat ventral tegmental neurones in vitro studied by intracellular recording. Br J Pharmacol 98: 135-140.
7. Carlson JH, Foote SL (1992) Oscillation of interspike interval length in substantia nigra dopamine neurons: effects of nicotine and the dopaminergic D2 agonist LY 163502 on electrophysiological activity. Synapse 11: 229-248.
8. Charpantier E, Barneoud P, Moser P, Besnard F, Sgard F (1998) Nicotinic acetylcholine subunit mRNA expression in dopaminergic neurons of the rat substantia nigra and ventral tegmental area. Neuroreport 9: 3097-3101.
9. Chergui K, Suaud-Chagny MF, Gonon F (1994) Nonlinear relationship between impulse flow, dopamine release and dopamine elimination in the rat brain in vivo. Neuroscience 62: 641-645.
10. Clarke PB, Pert A (1985) Autoradiographic evidence for nicotine receptors on nigrostriatal and mesolimbic dopaminergic neurons. Brain Res 348: 355-358.
11. Dani JA, Heinemann S (1996) Molecular and cellular aspects of nicotine abuse. Neuron 16: 905-908.
12. Diana M, Tepper JM (2002) Electrophysiological pharmacology of mesencephalic dopaminergic neurons. In: Handbook of experimental pharmacology (Ed. G. DiChiara). Springer-Verlag, p. 1-61.
13. Enoch MA, Harris CR, Goldman D (2001) Does a reduced sensitivity to bitter taste increase the risk of becoming nicotine addicted? Addict Behav 26: 399-404.
14. Erhardt S, Oberg H, Engberg G (2001) Pharmacologically elevated levels of endogenous kynurenic acid prevent nicotine-induced activation of nigral dopamine neurons. Naunyn Schmiedebergs Arch Pharmacol 363: 21-27.
15. Fa M, Carcangiu G, Passino N, Ghiglieri V, Gessa GL, Mereu G (2000) Cigarette smoke inhalation stimulates dopaminergic neurons in rats. Neuroreport 11: 3637-3639.
16. Goldner FM, Dineley KT, Patrick JW (1997) Immunohistochemical localization of the nicotinic acetylcholine receptor subunit alpha6 to dopaminergic neurons in the substantia nigra and ventral tegmental area. Neuroreport 8: 2739-2742.
17. Gonon FG (1988) Nonlinear relationship between impulse flow and dopamine released by rat midbrain dopaminergic neurons as studied by in vivo electrochemistry. Neuroscience 24: 19-28.
18. Gonon FG, Buda MJ (1985) Regulation of dopamine release by impulse flow and by autoreceptors as studied by in vivo voltammetry in the rat striatum. Neuroscience 14: 765-774.
19. Grenhoff J, Aston-Jones G, Svensson TH (1986) Nicotinic effects on the firing pattern of midbrain dopamine neurons. Acta Physiol Scand 128: 351-358.
20. Grillner P, Svensson TH (2000) Nicotine-induced excitation of midbrain dopamine neurons in vitro involves ionotropic glutamate receptor activation. Synapse 38: 1-9.
21. Henderson Z, Sherriff FE (1991) Distribution of choline acetyltransferase immunoreactive axons and terminals in the rat and ferret brainstem. J Comp Neurol 314: 147-163.
22. Imperato A, Mulas A, Di Chiara G (1986) Nicotine preferentially stimulates dopamine release in the limbic system of freely moving rats. Eur J Pharmacol 132: 337-338.
23. Jacobowitz DM, Goldberg AM (1977) Determination of acetylcholine in discrete regions of the rat brain. Brain Res 122: 575-577.
24. Kaufman NJ, Castrucci BC, Mowery PD, Gerlach KK, Emont S, Orleans CT (2002) Predictors of change on the smoking uptake continuum among adolescents. Arch Pediatr Adolesc Med 156: 581-587.
25. Kendler KS, Neale MC, Sullivan P, Corey LA, Gardner CO, Prescott CA (1999) A population-based twin study in women of smoking initiation and nicotine dependence. Psychol Med 29: 299-308.
26. Keuthen NJ, Niaura RS, Borrelli B, Goldstein M, DePue J, Murphy C, Gastfriend D, Reiter SR, Abrams D (2000) Comorbidity, smoking behavior and treatment outcome. Psychother Psychosom 69: 244-250.
27. Kitai ST, Shepard PD, Callaway JC, Scroggs R (1999) Afferent modulation of dopamine neuron firing patterns. Curr Opin Neurobiol 9: 690-697.
28. Klink R, de Kerchove d'Exaerde A, Zoli M, Changeux JP (2001) Molecular and physiological diversity of nicotinic acetylcholine receptors in the midbrain dopaminergic nuclei. J Neurosci 21: 1452-1463.
29. Lavoie B, Parent A (1994) Pedunculopontine nucleus in the squirrel monkey: cholinergic and glutamatergic projections to the substantia nigra. J Comp Neurol 344: 232-241.
30. Lichtensteiger W, Felix D, Lienhart R, Hefti F (1976) A quantitative correlation between single unit activity and fluorescence intensity of dopamine neurones in zona compacta of substantia nigra, as demonstrated under the influence of nicotine and physostigmine. Brain Res 117: 85-103.
31. Lichtensteiger W, Hefti F, Felix D, Huwyler T, Melamed E, Schlumpf M (1982) Stimulation of nigrostriatal dopamine neurones by nicotine. Neuropharmacology 21: 963-968.
32. Mansvelder HD, Keath JR, McGehee DS (2002) Synaptic mechanisms underlie nicotine-induced excitability of brain reward areas. Neuron 33: 905-919.
33. Martinez-Murillo R, Villalba R, Montero-Caballero MI, Rodrigo J (1989) Cholinergic somata and terminals in the rat substantia nigra: an immunocytochemical study with optical and electron microscopic techniques. J Comp Neurol 281: 397-415.
34. Massey SC, James TA (1978) The uptake of 3H-choline and release of 3H-acetylcholine in the rat substantia nigra. Life Sci 23: 345-350.
35. Mereu G, Yoon KW, Boi V, Gessa GL, Naes L, Westfall TC (1987) Preferential stimulation of ventral tegmental area dopaminergic neurons by nicotine. Eur J Pharmacol 141: 395-399.
36. Nestler EJ (1992) Molecular mechanisms of drug addiction. J Neurosci 12: 2439-2450.
37. Nisell M, Nomikos GG, Svensson TH (1994a) Infusion of nicotine in the ventral tegmental area or the nucleus accumbens of the rat differentially affects accumbal dopamine release. Pharmacol Toxicol 75: 348-352.
38. Nisell M, Nomikos GG, Svensson TH (1994b) Systemic nicotine-induced dopamine release in the rat nucleus accumbens is regulated by nicotinic receptors in the ventral tegmental area. Synapse 16: 36-44.
39. 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.
40. Overton PG, Clark D (1997) Burst firing in midbrain dopaminergic neurons. Brain Res Brain Res Rev 25: 312-334.
41. Pianezza ML, Sellers EM, Tyndale RF (1998) Nicotine metabolism defect reduces smoking. Nature 393: 750.
42. Picciotto MR, Zoli M, Rimondini R, Lena C, Marubio LM, Pich EM, Fuxe K, Changeux JP (1998) Acetylcholine receptors containing the beta2 subunit are involved in the reinforcing properties of nicotine. Nature 391: 173-177.
43. Pidoplichko VI, DeBiasi M, Williams JT, Dani JA (1997) Nicotine activates and desensitizes midbrain dopamine neurons. Nature 390: 401-404.
44. Simon TR, Sussman S, Dent CW, Burton D, Flay BR (1995) Prospective correlates of exclusive or combined adolescent use of cigarettes and smokeless tobacco: a replication-extension. Addict Behav 20: 517-524.
45. Sorenson EM, Shiroyama T, Kitai ST (1998) Postsynaptic nicotinic receptors on dopaminergic neurons in the substantia nigra pars compacta of the rat. Neuroscience 87: 659-673.
46. Spitz MR, Shi H, Yang F, Hudmon KS, Jiang H, Chamberlain RM, Amos CI, Wan Y, Cinciripini P, Hong WK, Wu X (1998) Case-control study of the D2 dopamine receptor gene and smoking status in lung cancer patients. J Natl Cancer Inst 90: 358-363.
47. Suaud-Chagny MF, Chergui K, Chouvet G, Gonon F (1992) 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: 63-72.
48. Tickle JJ, Sargent JD, Dalton MA, Beach ML, Heatherton TF (2001) Favourite movie stars, their tobacco use in contemporary movies, and its association with adolescent smoking. Tob Control 10: 16-22.
49. Tsuneki H, Klink R, Lena C, Korn H, Changeux JP (2000) Calcium mobilization elicited by two types of nicotinic acetylcholine receptors in mouse substantia nigra pars compacta. Eur J Neurosci 12: 2475-2485.
50. Wada E, Wada K, Boulter J, Deneris E, Heinemann S, Patrick J, Swanson LW (1989) Distribution of alpha2, alpha3, alpha4, and beta2 neuronal nicotinic receptor subunit mRNAs in the central nervous system: a hybdrization histochemical study in the rat. J Comp Neurol 284: 314-335.
51. Werkman TR, Kruse CG, Nievelstein H, Long SK, Wadman WJ (2001) In vitro modulation of the firing rate of dopamine neurons in the rat substantia nigra pars compacta and the ventral tegmental area by antipsychotic drugs. Neuropharmacology 40: 927-936.
52. Woolf AD (1997) Smoking and nicotine addiction: a pediatric epidemic with sequelae in adulthood. Curr Opin Pediatr 9: 470-477.
53. Wooltorton JRA, Pidoplichko VI, Broide RS, Dani JA (2003) Differential desensitization and distribution of nicotinic acetylcholine receptor subtypes in midbrain dopamine areas. J Neurosci 23: 3176-3185.
54. Yin R, French ED (2000) A comparison of the effects of nicotine on dopamine and non-dopamine neurons in the rat ventral tegmental area: an in vitro electrophysiological study. Brain Res Bull 51: 507-514.
55. Zeman MV, Hiraki L, Sellers EM (2002) Gender differences in tobacco smoking: higher relative exposure to smoke than nicotine in women. J Womens Health Gend Based Med 11: 147-153.