The effects of nicotine on neural pathways implicated in depression: A factor in nicotine addiction

Pharmacology Biochemistry and Behavior

Volumn 66, Issue 1, 2000, Pages 79-85

  Balfour, David J K ^a   Ridley, Diana L ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

Depression; Hippocampal 5 HT; Mesolimbic dopamine; Nicotine dependence

Indexed keywords

DOPAMINE; NICOTINE; SEROTONIN;

ARTICLE; DEPRESSION; FOREBRAIN; HIPPOCAMPUS; LIMBIC CORTEX; MENTAL STRESS; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; SMOKING; SUBSTANCE ABUSE; TOBACCO;

ANIMALS; ANTIDEPRESSIVE AGENTS; BRAIN; DEPRESSION; DOPAMINE; HUMANS; NICOTINE; SEROTONIN; SMOKING; TOBACCO USE DISORDER;

ANIMALIA; NICOTIANA TABACUM;

EID: 0034029806     PISSN: 00913057     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0091-3057(00)00205-7     Document Type: Article

References (89)

1. Ahmed S.H., Koob G.F. Cocaine, but not food-seeking behavior is reinstated by stress after extinction. Psychopharmacology (Berlin). 132:1997;289-295.
2. Ainsworth K., Smith S.E., Zetterstrom T.S., Pei Q., Sharp T. Effect of antidepressant drugs on dopamine D1 and D2 receptor expression and dopamine release in the nucleus accumbens of the rat. Psychopharmacology (Berlin). 140:1998;470-477.
3. Andrews N., File S.E., Fernandez C., Gonzales L.E., Barnes N.M. Evidence that the median raphe nucleus-dorsal hippocampal pathway mediate diazepam withdrawal-induced anxiety. Psychopharmacology (Berlin). 130:1997;228-234.
4. Aubin H.J., Tilikete S., Barrucand D. Depression and smoking. Encephalé 22:1996;17-22.
5. Azmitia E.C., Segal M. An autoradiographic analysis of the differential ascending projections of the dorsal and median raphe nuclei of the rat. J. Comp. Neurol. 179:1978;641-668.
6. Balfour D.J.K. A comparison of the effects of nicotine and (+)-amphetamine on rat behaviour an unsignalled Sidman avoidance schedule. J. Pharm. Pharmacol. 42:1990;257-260.
7. Balfour D.J.K. The influence of stress on psychopharmacological responses to nicotine. Br. J. Addict. 86:1991;489-493.
8. Balfour D.J.K., Benwell M.E.M., Birrell C.E., Kelly R.J., Al-Aloul M. Sensitization of the mesoaccumbens dopamine response to nicotine. Pharmacol. Biochem. Behav. 59:1998;1021-1030.
9. Balfour D.J.K., Fagerström K.O. Pharmacology of nicotine and its therapeutic use in smoking cessation and neurodegenerative disorders. Pharmacol. Ther. 72:1996;1-81.
10. Balfour D.J.K., Graham C.A., Vale A.L. Studies on the possible role of brain 5-HT systems and adrenocortical activity in behavioural responses to nicotine and diazepam. Psychopharmacology (Berlin). 90:1986;528-532.
11. Balfour D.J.K., Reid A. Effects of betamethasone on the stimulation of corticosterone secretion in rats. Arch. Int. Pharmacodyn. Ther. 237:1979;67-74.
12. Barden N., Reul J.M.H.M., Holsboer F. Do antidepressants stabilize mood through actions on the hypothalamic-pituitary-adrenocortical system. Trends Neurosci. 18:1995;6-10.
13. Benowitz N.L. Acute biological effects of nicotine and its metabolites. Clarke P.B.S., Quik M., Adlkofer F., Thurau K. Effects of nicotine on biological systems II. 1994;9-16 Birkhäuser Verlag, Basel.
14. Benwell M.E.M., Balfour D.J.K. Effects of nicotine and its withdrawal on plasma corticosterone and brain 5-hydroxyindoles. Psychopharmacology (Berlin). 63:1979;7-11.
15. Benwell M.E.M., Balfour D.J.K. Effects of chronic nicotine administration on the response and adaptation to stress. Psychopharmacology (Berlin). 76:1982;160-162.
16. Benwell M.E.M., Balfour D.J.K. Effects of nicotine administration on the uptake and biosynthesis of 5-HT in rat brain synaptosomes. Eur. J. Pharmacol. 84:1982;71-77.
17. Benwell M.E.M., Balfour D.J.K. The effects of acute and repeated nicotine treatment on nucleus accumbens dopamine and locomotor activity. Br. J. Pharmacol. 105:1992;849-856.
18. Benwell M.E.M., Balfour D.J.K. Regional variation in the effects of nicotine on catecholamine overflow in the rat brain. Eur. J. Pharmacol. 325:1997;13-20.
19. Benwell M.E.M., Balfour D.J.K., Anderson J.M. Smoking-associated changes in the serotonergic systems of discrete regions of human brain. Psychopharmacology (Berlin). 102:1990;68-72.
20. Benwell M.E.M., Balfour D.J.K., Birrell C.E. Desensitisation of nicotine-induced dopamine responses during constant infusion with nicotine. Br. J. Pharmacol. 114:1995;211-217.
21. Benwell M.E.M., Balfour D.J.K., Lucchi H.M. The influence of tetrodotoxin and calcium on the stimulation of mesolimbic dopamine activity evoked by systemic nicotine. Psychopharmacology (Berlin). 112:1993;467-471.
22. Berridge K.C., Robinson T.E. What is the role of dopamine in reward. Hedonic impact, reward learning or incentive salience Brain Res. Rev. 28:1998;309-369.
23. Biagini G., Pich E.M., Carani C., Marrama P., Agnati L.F. Postnatal maternal separation during the stress hyporesponsive period enhances the adrenocortical response to novelty in adult rats by affecting feedback regulation in the CA1 hippocampal field. Int. J. Dev. Neurosci. 16:1998;187-197.
24. Birnsteil S., List T.J., Beck S.G. Chronic corticosterone treatment maintains synaptic activity of CA1 hippocampal pryramidal cells. Acute high corticosterone administration increases action potential number Synapse. 20:1995;117-124.
25. Birrell C.E., Balfour D.J.K. The influence of nicotine pretreatment on mesoaccumbens dopamine overflow and locomotor responses to D-amphetamine. Psychopharmacology (Berlin). 140:1998;142-149.
26. Breslau N., Kilber M.M., Andreski P. Nicotine dependence and major depression. Arch. Gen. Psychiatry. 50:1993;31-35.
27. Brioni J.D., O’Neil A.B., Kim D.J.B., Buckley M.J., Decker M.W., Arneric S.P. Anxiolytic-like effects of the novel cholinergic channel activator ABR-418. J. Pharmacol. Exp. Ther. 271:1994;352-361.
28. Buczek Y., Lê A.D., Wang A., Stewart J., Shaham Y. Stress reinstates nicotine seeking but not sucrose solution seeking in rats. Psychopharmacology (Berlin). 144:1999;183-188.
29. Burrows G.D., Maguire K.P., Norman T.R. Antidepressant efficacy and tolerability of the selective norepinephrine reuptake inhibitor reboxetine. A review J. Clin. Psychiatry. 59(Suppl. 14):1998;4-7.
30. Chiamulera C., Borgo C., Falchetto S., Valerio E., Tessari M. Nicotine reinstatement of nicotine self-administration after long-term extinction. Psychopharmacology (Berlin). 127:1996;102-107.
31. Clarke P.B.S., Fu D.S., Jakubovic A., Fibiger H.C. Evidence that mesolimbic dopaminergic activation underlies the locomotor stimulant action of nicotine in rats. J. Pharmacol. Exp. Ther. 246:1988;701-708.
32. 2 receptors in chronic fluoxetine-treated rats. Eur. J. Pharmacol. 322:1997;123-127.
33. Cooper B.R., Hester T.J., Maxwell R.A. Behavioral and biochemical effects of the antidepressant, bupropion (Wellbutin). Evidence for selective blockade of dopamine uptake in vivo J. Pharmacol. Exp. Ther. 215:1980;127-134.
34. Copland A.M., Balfour D.J.K. The effects of diazepam on brain 5-HT and 5-HIAA in stressed and unstressed rats. Pharmacol. Biochem. Behav. 27:1987;619-624.
35. Cornelius J.R., Salloum I.M., Ehler J.G., Jarrett P.J., Cornelius M.D., Black A., Perel J.M., Thase M.E. Double blind fluoxetine in depressed alcoholic patients. Psychopharmacol. Bull. 33:1997;165-170.
36. Corrigall W.A., Coen K.M., Adamson K.L. Self-administered nicotine activates the mesolimbic dopamine system through the ventral tegmental area. Brain. Res. 653:1994;278-284.
37. Corrigall W.A., Franklin K.J.B., Coen K.M., Clarke P.B.S. The mesolimbic dopaminergic system is implicated in the reinforcing effects of nicotine. Psychopharmacology (Berlin). 107:1992;285-289.
38. Costall B., Kelly M.E., Naylor R.J., Onaivi E.S. The actions of nicotine and cocaine in a mouse model of anxiety. Pharmacol. Biochem. Behav. 33:1989;197-203.
39. Covey L.S., Glassman A.H., Stetner F. Cigarette smoking and major depression. J. Addict. Res. 17:1998;35-46.
40. Deakin J.F.W., Graeff F.G. 5-HT and mechanisms of defence. J. Psychopharmacol. 5:1991;305-315.
41. Di Chiara G. A motivational learning hypothesis of the role of mesolimbic dopamine in compulsive drug use. J. Psychopharmacol. 12:1998;54-67.
42. Di Chiara G. Drug addiction as a dopamine-dependent associative learning disorder. Eur. J. Pharmacol. 375:1999;13-30.
43. Di Chiara G., Imperato A. Drugs abused by humans preferentially increase synaptic dopamine concentrations in the mesolimbic system of freely moving rats. Proc. Natl. Acad. Sci. USA. 85:1988;5274-5278.
44. Doherty K., Kinnune T., Militello F.S., Garvey A.J. Urges to smoke during the first month of abstinence. Relationship to relapse and predictors Psychopharmacology (Berlin). 119:1995;171-178.
45. Epping-Jordan M.P., Watkins S.S., Koob G.F., Markou A. Dramatic decreases in brain reward function during nicotine withdrawal. Nature. 393:1998;76-79.
46. File S.E., Kenny P.J., Ouagazzal A.-M. Anxiolytic and anxiogenic effects of nicotine in the social interaction test. Role of the dorsal hippocampus Behav. Neurosci. 112:1998;1423-1429.
47. Fowler J.S., Volkow N.D., Wang G.-J., Pappas N., Logan J., Shea C., Alexoff D., MacGregor R.R., Schyler D.J., Zezulkova I., Wolf A.P. Brain monoamine oxidase A inhibition in cigarette smokers. Proc. Natl. Acad. Sci. USA. 93:1996;14065-14069.
48. Fowler J.S., Volkow N.D., Wang G.-J., Pappas N., Logan J., MacGregor R., Alexoff D., Shea C., Schyler D., Wolf A.P., Warner D., Zezulkova I., Cilento R. Inhibition of monoamine oxidase B in the brains of smokers. Nature. 379:1996;733-736.
49. Fowler J.S., Volkow N.D., Logan J., Pappas N., King P., MacGregor R.R., Shea C, Garza V., Gatley S.J. An acute dose of nicotine does not inhibit MAO B in baboon brain in vivo. Life Sci. 63:1998;PL19-PL23.
50. Gilbert D.G. Paradoxical tranquilizing and emotion-reducing effects of nicotine. Psychol. Bull. 86:1979;643-661.
51. Graeff F.G., Guimaraes F.S., De Andrade T.G., Deakin J.F. Role of 5-HT in stress, anxiety and depression. Pharmacol. Biochem. Behav. 54:1996;114-129.
52. Hildebrand B.E., Nomikos G.G., Hertel P., Schilström B., Svensson T.H. Reduced dopamine output in the nucleus accumbens but not the medial prefrontal cortex in rats displaying a mecamylamine-precipitated nicotine withdrawal syndrome. Brain Res. 779:1998;214-225.
53. Hughes J.R., Goldstein M.G., Hurt R.D., Schiffman S. Recent advances in the pharmacotherapy of smoking. JAMA. 281:1999;72-76.
54. Hughes J.R., Higgins S.T., Bickel W.K. Nicotine withdrawal versus other drug withdrawal syndromes. Similarities and dissimilarities Addiction. 89:1994;1461-1470.
55. Imperato A., Mulas A., Di Chiara G. Nicotine preferentially stimulates dopamine release in the limbic system of freely moving rats. Eur. J. Pharmacol. 132:1986;337-338.
56. Kapur S., Mann J.J. Role of dopamine systems in depression. Biol. Psychiatry. 32:1992;1-17.
57. 2-receptors. J. Pharm. Pharmacol. 41:1989;555-558.
58. Lê A.D., Quan B., Juzystch W., Kletcher P.J., Joharchi N., Shaham Y. Reinstatement of alcohol-seeking by priming injections of alcohol and exposure to stress in rats. Psychopharmacology (Berlin). 135:1998;169-174. -.
59. Lehr E. Testing antipsychotic drug effects with operant procedures. Hoffmeister F., Stille G. Handbook of experimental pharmacology, vol. 55 (part 1). 1980;90-95 Springer Verlag, Berlin.
60. Louis M., Clarke P.B.S. Effect of ventral tegmental 6-hydroxydopamine lesions on the locomotor stimulant action of nicotine in rats. Neuropharmacology. 37:1998;1503-1513.
61. 3 receptors in the rat brain. Eur. J. Pharmacol. 351:1998;31-37.
62. Maj J., Wedzony K., Klimek V. Desipramine given repeatedly enhances behavioural effects of dopamine and d-amphetamine injected into the nucleus accumbens. Eur J. Pharmacol. 140:1987;179-185.
63. Markou A., Kosten T.R., Koob G.F. Neurobiological similarities in depression and drug dependence. A self-medication hypothesis Neuropharmacology. 18:1998;135-174.
64. Meany M.J., Aitken D.H., Viau V., Sharma S., Sarrieau A. Neonatal handling alters adrenocortical negative feedback sensitivity and hippocampal type-II glucocorticoid receptor-binding in the rat. Neuroendocrinology. 50:1989;597-604.
65. Mitchell S.N. Role of the locus coeruleus in the noradrenergic response to a systemic administration of nicotine. Neuropharmacology. 32:1993;937-949.
66. Morrison C.F. Effects of nicotine and its withdrawal on the performance of rats on signalled and unsignalled avoidance schedules. Psychopharmacologia. 38:1974;25-35.
67. Nomikos G.G., Damsma G., Wenkster D., Fibiger H.C. Chronic desipramine enhances amphetamine-induced increases in interstitial concentrations of dopamine in the nucleus accumbens. Eur. J. Pharmacol. 195:1991;63-73.
68. Nomikos G.G., Zis A.O.P., Damsma G., Fibiger H.C. Effects of chronic electroconvulsive shock on interstitial concentrations of dopamine in the nucleus accumbens. Psychopharmacology (Berlin). 105:1991;230-238.
69. Ouagazzal A.-M., Kenny P.J., File S.E. Modulation of behaviour on trials 1 and 2 in the elevated plus-maze test of anxiety after systemic and hippocampal administration of nicotine. Psychopharmacology (Berlin). 144:1999;54-60.
70. Paxinos G., Watson C. The rat brain in sterotaxic coordinates. 1986;Academic Press, Sydney.
71. Piazza P.V., Le Moal M. Glucocorticoids as a biological substrate of reward. Physiological and pathophysiological implications Brain Res. Rev. 25:1997;359-372.
72. Piazza P.V., Le Moal M. The role of stress in drug self-administration. Trends Pharmacol. Sci. 19:1998;67-74.
73. Pidoplichko V., De Bias M., Williams J.T., Dani J. Nicotine activates and desensitizes midbrain dopamine neurones. Nature. 390:1997;401-404.
74. Plaznik A., Kostowski W. The effects of antidepressants and electroconvulsive shocks on the functioning of the mesolimbic dopamine system. A behavioral study Eur. J. Pharmacol. 135:1987;389-396.
75. Pomerleau C.S., Pomerleau O.F. The effects of a psychological stressor on cigarette smoking and subsequent behavioral and physiological responses. Psychophysiology. 24:1987;274-285.
76. Pontieri F., Tanda G., Orzi F., Di Chiara G. Effects of nicotine on the nucleus accumbens and similarity to those of addictive drugs. Nature. 382:1996;255-257.
77. Porsolt R.D., Anton G., Blavet N., Jalfre M. Behavioural despair in rats. A new model sensitive to antidepressant treatments Eur. J. Pharmacol. 47:1978;379-391.
78. Ribeiro E.B., Bettiker R.L., Bogdanov M., Wurtman R.J. Effects of systemic nicotine on serotonin release in rat brain. Brain Res. 621:1993;311-318.
79. Russell M.A.H. Nicotine intake and its control over smoking. Wonnacott S., Russell M.A.H., Stolerman I.P. Nicotine psychopharmacology. Molecular, cellular and behavioural aspects:1990;374-418 Oxford University Press, Oxford.
80. Salin-Pascual R.J., Rosas M., Jimenez-Genchi A., Rivera-Meza B.L., Delgado-Parra V. Antidepressant effect of transdermal nicotine patches in nonsmoking patients with major depression. J. Clin. Psychiatry. 57:1996;387-389.
81. Seckl J.R., Fink G. Use of in situ hybridization to investigate the regulation of hippocampal corticosteroid receptors by monoamines. J. Steroid. Biochem. Mol. Biol. 40:1991;685-688.
82. Semba J., Mataki C., Yamada S., Nankai M., Toru M. Antidepressant-like effects of chronic nicotine on learned helplessness paradigm in rats. Biol. Psychiatry. 43:1998;389-391.
83. Shaham Y., Stewart J. Stress reinstates heroin self-administration behavior in drug-free animals. An effect mimicking heroin but not withdrawal Psychopharmacology (Berlin). 119:1995;334-341.
84. Shiffman S., Hickcox M., Paty J.A., Gnys M., Kassel J.D., Richards T.J. Progression from a smoking lapse to relapse. Prediction from abstinence violation effects, nicotine dependence and lapse characteristics J. Consult. Clin. Psychol. 64:1996;993-1002.
85. 2-like dopamine receptors. Psychopharmacology (Berlin). 133:1997;77-84.
86. Stolerman I.P., Shoaib M. The neurobiology of tobacco addiction. Trends Pharmacol. Sci. 12:1991;467-473.
87. Vale A.L., Balfour D.J.K. Aversive environmental stimuli as a factor in the psychostimulant response to nicotine. Pharmacol. Biochem. Behav. 32:1989;857-860.
88. Wise R.A., Bozarth M.A. A psychomotor stimulant theory of addiction. Psychol. Rev. 94:1987;469-492.
89. Yau J.L., Kelly P.A., Seckl J.R. Increased glucocorticoid gene expression in the rat hippocampus following combined serotonergic and medial septal cholinergic lesions. Mol. Brain Res. 27:1994;174-178.