Modulation of ventral tegmental area dopamine receptors inhibit nicotine-induced anxiogenic-like behavior in the central amygdala

Progress in Neuro-Psychopharmacology and Biological Psychiatry

Volumn 41, Issue , 2013, Pages 11-17

  Zarrindast, Mohammad Reza ^a,b,c,d   Eslahi, Nafiseh ^e   Rezayof, Ameneh ^f   Rostami, Parvin ^e   Zahmatkesh, Maryam ^a  

^a TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^c INSTITUTE FOR RESEARCH IN FUNDAMENTAL SCIENCES IPM   (Iran)

^d Institute of Cognitive Science Studies (ICSS)   (Iran)

^e KHARAZMI UNIVERSITY   (Iran)

^f UNIVERSITY OF TEHRAN   (Iran)

Author keywords

Anxiety; Central amygdala; Elevated plus maze; Nicotine; Ventral tegmental area

Indexed keywords

8 CHLORO 2,3,4,5 TETRAHYDRO 3 METHYL 5 PHENYL 1H 3 BENZAZEPIN 7 OL HYDROGEN MALEATE; DOPAMINE 1 RECEPTOR; DOPAMINE 2 RECEPTOR; DOPAMINE 3 RECEPTOR; DOPAMINE RECEPTOR BLOCKING AGENT; SULPRIDE; UNCLASSIFIED DRUG;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY; ARTICLE; CENTRAL NUCLEUS (AMYGDALA); CONTROLLED STUDY; DOPAMINE RELEASE; DOPAMINERGIC TRANSMISSION; HISTOPATHOLOGY; INHIBITION (PSYCHOLOGY); LOCOMOTION; MALE; MAZE TEST; NEUROMODULATION; NEUROPHYSIOLOGY; NONHUMAN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; TASK PERFORMANCE; VENTRAL TEGMENTUM;

AMYGDALA; ANIMALS; ANXIETY; BENZAZEPINES; DOPAMINE ANTAGONISTS; INJECTIONS, INTRAVENTRICULAR; MALE; NICOTINE; RATS; RATS, WISTAR; RECEPTORS, DOPAMINE; RECEPTORS, DOPAMINE D1; RECEPTORS, DOPAMINE D2; RECEPTORS, DOPAMINE D3; SULPIRIDE; VENTRAL TEGMENTAL AREA;

EID: 84870824660     PISSN: 02785846     EISSN: 18784216     Source Type: Journal    
DOI: 10.1016/j.pnpbp.2012.09.004     Document Type: Article

References (72)

1. Adell A., Artigas F. The somatodendritic release of dopamine in the ventral tegmental area and its regulation by afferent transmitter systems. Neurosci Biobehav Rev 2004, 28:415-431.
2. Ariano M.A., Wang J., Noblett K.L., Larson E.R., Sibley D.R. Cellular distribution of the rat D1B receptor in central nervous system using anti-receptor antisera. Brain Res 1997, 23(746):141-150.
3. Barazangi N., Role L.W. Nicotine-induced enhancement of glutamatergic and GABAergic synaptic transmission in the mouse amygdala. J Neurophysiol 2001, 86:463-474.
4. Benowitz N.L. Neurobiology of nicotine addiction: implications for smoking cessation treatment. Am J Med 2008, 121:S3-S10.
5. Björklund A., Lindvall O. Dopamine in dendrites of substantia nigra neurons: suggestions for a role in dendritic terminals. Brain Res 1975, 17(83):531-537.
6. Brunzell D.H., Russell D.S., Picciotto M.R. In vivo nicotine treatment regulates mesocorticolimbic CREB and ERK signaling in C57BL/6J mice. J Neurochem 2003, 84:1431-1441.
7. Carobrez A.P., Bertoglio L.J. Ethological and temporal analyses of anxiety-like behavior: the elevated plus-maze model 20 years on. Neurosci Biobehav Rev 2005, 29:1193-1205.
8. Cassell M.D., Gray T.S., Kiss J.Z. Neuronal architecture in the rat central nucleus of the amygdala: a cytological, hodological and immunocytochemical study. J Comp Neurol 1986, 246:478-499.
9. Chen B.T., Rice M.E. Synaptic regulation of somatodendritic dopamine release by glutamate and GABA differs between substantia nigra and ventral tegmental area. J Neurochem 2002, 81:158-169.
10. Corrigall W.A., Franklin K.B., Coen K.M., Clarke P.B. The mesolimbic dopaminergic system is implicated in the reinforcing effects of nicotine. Psychopharmacology (Berl) 1992, 107:285-289.
11. Corrigall W.A., Coen K.M., Adamson K.L. Self-administered nicotine activates the mesolimbic dopamine system through the ventral tegmental area. Brain Res 1994, 653:278-284.
12. Dajas-Bailador F., Wonnacott S. Nicotinic acetylcholine receptors and the regulation of neuronal signalling. Trends Pharmacol Sci 2004, 25:317-324.
13. David V., Besson M., Changeux J.P., Granon S., Cazala P. Reinforcing effects of nicotine microinjections into the ventral tegmental area of mice: dependence on cholinergic nicotinic and dopaminergic D1 receptors. Neuropharmacology 2006, 50:1030-1040.
14. de la Mora M.P., Gallegos-Cari A., Arizmendi-García Y., Marcellino D., Fuxe K. Role of dopamine receptor mechanisms in the amygdaloid modulation of fear and anxiety: structural and functional analysis. Prog Neurobiol 2010, 90:198-216.
15. Di Chiara G. Role of dopamine in the behavioural actions of nicotine related to addiction. Eur J Pharmacol 2000, 393:295-314.
16. Fletcher P.J., Dzung Le A., Higgins G.A. Serotonin receptors as potential targets for modulation of nicotine use and dependence. Prog Brain Res 2008, 172.
17. Foulds J., Stapleton J.A., Bell N., Swettenham J., Jarvis M.J., Russell M.A. Mood and physiological effects of subcutaneous nicotine in smokers and never-smokers. Drug Alcohol Depend 1997, 44:105-115.
18. Fu Y., Matta S.G., James T.J., Sharp B.M. Nicotine-induced norepinephrine release in the rat amygdala and hippocampus is mediated through brainstem nicotinic cholinergic receptors. J Pharmacol Exp Ther 1998, 284:1188-1196.
19. Fu Y., Matta S.G., Gao W., Brower V.G., Sharp B.M. Systemic nicotine stimulates dopamine release in nucleus accumbens: re-evaluation of the role of N-methyl-d-aspartate receptors in the ventral tegmental area. J Pharmacol Exp Ther 2000, 294:458-465.
20. Fudge J.L., Haber S.N. The central nucleus of the amygdala projection to dopamine subpopulations in primates. Neuroscience 2000, 97:479-494.
21. Gelowitz D.L., Kokkinidis L. Enhanced amygdala kindling after electrical stimulation of the ventral tegmental area: implications for fear and anxiety. J Neurosci 1999, 15(19):RC41.
22. Grenhoff J., Aston-Jones G., Svensson T.H. Nicotinic effects on the firing pattern of midbrain dopamine neurons. Acta Physiol Scand 1986, 128:351-358.
23. Herrera D.G., Robertson H.A. Activation of c-fos in the brain. Prog Neurobiol 1996, 50:83-107.
24. Hopkins D.A. Amygdalotegmental projections in the rat, cat and rhesus monkey. Neurosci Lett 1975, 1:263-270.
25. Hyttel J. SCH 23390: the first selective dopamine D1 antagonist. Eur J Pharmacol 1983, 91:153-154.
26. Ikemoto S., Qin M., Liu Z.H. Primary reinforcing effects of nicotine are triggered from multiple regions both inside and outside the ventral tegmental area. J Neurosci 2006, 26:723-730.
27. Iorio L.C., Barnett A., Leitz F.H., Houser V.P., Korduba C.A. SCH23390, a potential benzazepine antipsychotic with unique interactions on dopaminergic systems. J Pharmacol Exp Ther 1983, 226:462-468.
28. Ishii K., Wong J.K., Sumikawa K. Comparison of alpha2 nicotinic acetylcholine receptor subunit mRNA expression in the central nervous system of rats and mice. J Comp Neurol 2005, 493:241-260.
29. Kalin N.H., Shelton S.E., Davidson R.J. The role of the central nucleus of the amygdala in mediating fear and anxiety in the primate. J Neurosci 2004, 24:5506-5515.
30. Kalivas P.W., Duffy P. D1 receptors modulate glutamate transmission in the ventral tegmental area. J Neurosci 1995, 15:5379-5388.
31. Koga E., Momiyama T. Presynaptic dopamine D2-like receptors inhibit excitatory transmission onto rat ventral tegmental dopaminergic neurones. J Physiol 2000, 523:163-173.
32. Koob G.F. Dopamine, addiction and reward. Semin Neurosci 1992, 4:139-148.
33. Lanteri C., Salomon L., Torrens Y., Glowinski J., Tassin J.P. Drugs of abuse specifically sensitize noradrenergic and serotonergic neurons via a non-dopaminergic mechanism. Neuropsychopharmacology 2008, 33:1724-1734.
34. Lee H.J., Wheeler D.S., Holland P.C. Interactions between amygdala central nucleus and the ventral tegmental area in the acquisition of conditioned cue-directed behavior in rats. Eur J Neurosci 2011, 33:1876-1884.
35. Lesscher H.M., McMahon T., Lasek A.W., Chou W.H., Connolly J., Kharazia V., et al. Amygdala protein kinase C epsilon regulates corticotropin-releasing factor and anxiety-like behavior. Genes Brain Behav 2008, 7:323-333.
36. Li W., Doyon W.M., Dani J.A. Acute in vivo nicotine administration enhances synchrony among dopamine neurons. Biochem Pharmacol 2011, 15:977-983.
37. Lister R.G. Ethologically-based animal models of anxiety disorders. Pharmacol Ther 1990, 46:321-340.
38. Mansour A., Meador-Woodruff J.H., Bunzow J.R., Civelli O., Akil H., Watson S.J. Localization of D2 receptor mRNA and D1 and D2 receptor binding sites in the rat brain and pituitary: an in situ hybridization receptor autoradiographic analysis. J Neurosci 1990, 10:2587-2600.
39. Mansvelder H.D., Mertz M., Role L.W. Nicotinic modulation of synaptic transmission and plasticity in cortico-limbic circuits. Semin Cell Dev Biol 2009, 20:432-440.
40. Margolis E.B., Lock H., Hjelmstad G.O., Fields H.L. The ventral tegmental area revisited: is there an electrophysiological marker for dopaminergic neurons?. J Physiol 2006, 577:907-924.
41. Margolis E.B., Mitchell J.M., Ishikawa J., Hjelmstad G.O., Fields H.L. Midbrain dopamine neurons: projection target determines action potential duration and dopamine D(2) receptor inhibition. J Neurosci 2008, 28:8908-8913.
42. Markou A. Neurobiology of nicotine dependence. Philos Trans R Soc Lond B Biol Sci 2008, 363:3159-3168.
43. Matta S.G., Balfour D.J., Benowitz N.L., Boyd R.T., Buccafusco J.J., Caggiula A.R., et al. Guidelines on nicotine dose selection for in vivo research. Psychopharmacology 2007, 190:269-319.
44. Millan M.J., Newman-Tancredi A., Quentric Y., Cussac D. The "selective" dopamine D1 receptor antagonist, SCH23390, is a potent and high efficacy agonist at cloned human serotonin2C receptors. Psychopharmacology (Berl) 2001, 156:58-62.
45. Momiyama T., Sasa M., Takaori S. Enhancement of D2 receptor agonist-induced inhibition by D1 receptor agonist in the ventral tegmental area. Br J Pharmacol 1993, 110:713-718.
46. Pagliusi S.R., Tessari M., DeVevey S., Chiamulera C., Pich E.M. The reinforcing properties of nicotine are associated with a specific patterning of c-fos expression in the rat brain. Eur J Neurosci 1996, 8:2247-2256.
47. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 2007, Academic Press, New York.
48. Pellow S., File S.E. Anxiolytic and anxiogenic drug effects on exploratory activity in an elevated plus-maze: a novel test of anxiety in the rat. Pharmacol Biochem Behav 1986, 24:525-529.
49. Pellow S., Chopin P., File S.E., Briley M. Validation of open, closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J Neurosci Methods 1985, 14:149-167.
50. Phillips A.G., Ahn S., Howland J.G. Amygdalar control of the mesocorticolimbic dopamine system: parallel pathways to motivated behavior. Neurosci Biobehav Rev 2003, 27:543-554.
51. Picciotto M.R. Common aspects of the action of nicotine and other drugs of abuse. Drug Alcohol Depend 1998, 51:165-172.
52. Picciotto M.R. Nicotine as a modulator of behavior: beyond the inverted U. Trends Pharmacol Sci 2003, 24:493-499.
53. Pich E.M., Pagliusi S.R., Tessari M., Talabot-Ayer D., Hooft van Huijsduijnen R., et al. Common neural substrates for the addictive properties of nicotine and cocaine. Science 1997, 275:83-86.
54. Plaza-Zabala A., Martín-García E., de Lecea L., Maldonado R., Berrendero F. Hypocretins regulate the anxiogenic-like effects of nicotine and induce reinstatement of nicotine-seeking behavior. J Neurosci 2010, 10:2300-2310.
55. Price J.L., Amaral D.G. An autoradiographic study of the projections of the central nucleus of the monkey amygdala. J Neurosci 1981, 1:1242-1259.
56. Rahman S., McBride W.J. D1-D2 dopamine receptor interaction within the nucleus accumbens mediates long-loop negative feedback to the ventral tegmental area. J Neurochem 2001, 77:1248-1255.
57. Rice M.E., Cragg S.J., Greenfield S.A. Characteristics of electrically evoked somatodendritic dopamine release in substantia nigra and ventral tegmental area in vitro. J Neurophysiol 1997, 77:853-862.
58. Rodgers R.J., Johnson N.J.T. Factor analysis of spatiotemporal and ethological measures in the murine elevated plus-maze test of anxiety. Pharmacol Biochem Behav 1995, 52:297-303.
59. Role L.W., Berg D.K. Nicotinic receptors in the development and modulation of CNS synapses. Neuron 1996, 16:1077-1085.
60. Roozendaal B., McEwen B.S., Chattarji S. Stress, memory and the amygdala. Nat Rev Neurosci 2009, 10:423-433.
61. Rüther E., Degner D., Munzel U., Brunner E., Lenhard G., Biehl J., et al. Antidepressant action of sulpiride. Results of a placebo-controlled double blind trial. Pharmacopsychiatry 1999, 32:127-135.
62. Salminen O., Seppä T., Gäddnäs H., Ahtee L. The effects of acute nicotine on the metabolism of dopamine and the expression of Fos protein in striatal and limbic brain areas of rats during chronic nicotine infusion and its withdrawal. J Neurosci 1999, 19:8145-8151.
63. Schilstrom B., Rawal N., Mameli-Engvall M., Nomikos G.G., Svensson T.H. Dual effects of nicotine on dopamine neurons mediated by different nicotinic receptor subtypes. Int J Neuropsychopharmacol 2003, 6:1-11.
64. Sibley D.R., Monsma F.J., Shen Y. Molecular neurobiology of dopaminergic receptors. Int Rev Neurobiol 1993, 35:391-415.
65. Wallace D.M., Magnuson D.J., Gray T.S. Organization of amygdaloid projections to brainstem dopaminergic, noradrenergic and adrenergic cell groups in the rat. Brain Res Bull 1992, 28:447-454.
66. Wamsley J.K., Gehlert D.R., Filloux F.M., Dawson T.M. Comparison of the distribution of D-1 and D-2 dopamine receptors in the rat brain. J Chem Neuroanat 1989, 2:119-137.
67. White F.J., Wang R.Y. A10 dopamine neurons: role of autoreceptors in determining firing rate and sensitivity to dopamine agonists. Life Sci 1984, 34:1161-1170.
68. Xia Y., Driscoll J.R., Wilbrecht L., Margolis E.B., Fields H.L., Hjelmstad G.O. Nucleus accumbens medium spiny neurons target non-dopaminergic neurons in the ventral tegmental area. J Neurosci 2011, 31:7811-7816.
69. Yang K.C., Jin G.Z., Wu J. Mysterious alpha6-containing nAChRs: function, pharmacology, and pathophysiology. Acta Pharmacol Sin 2009, 30:740-751.
70. Yim C.Y., Mogenson G.J. Electrophysiological studies of neurons in the ventral tegmental area of Tsai. Brain Res 1980, 181:301-313.
71. Zarrindast M.R., Solati J., Oryan S., Parivar K. Effect of intra-amygdala injection of nicotine and GABA receptor agents on anxiety-like behaviour in rats. Pharmacology 2008, 82:276-284.
72. Zarrindast M.R., Naghdi-Sedeh N., Nasehi M., Sahraei H., Bahrami F., Asadi F. The effects of dopaminergic drugs in the ventral hippocampus of rats in the nicotine-induced anxiogenic-like response. Neurosci Lett 2010, 475:156-160.