Psychiatric disorders as vulnerability factors for nicotine addiction: What have we learned from animal models?

Current Topics in Behavioral Neurosciences

Volumn 24, Issue , 2015, Pages 155-170

  Foll, Bernard Le ^a,b   Ng, Enoch ^c   Ciano, Patricia Di ^a   Trigo, José M ^a  

^a CENTRE FOR ADDICTION AND MENTAL HEALTH   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c MOUNT SINAI HOSPITAL   (Canada)

Author keywords

Addiction; Anxiety; Mood disorders; Nicotine; Schizophrenia

Indexed keywords

CLOMIPRAMINE; DOPAMINE TRANSPORTER; MECAMYLAMINE; NICOTINIC RECEPTOR; SERTRALINE;

ANHEDONIA; ANXIETY DISORDER; ARTICLE; ATTENTION; CANNABIS ADDICTION; COGNITION; COGNITIVE DEFECT; COMORBIDITY; COPING BEHAVIOR; ELEVATED PLUS MAZE TEST; FORCED SWIM TEST; MENTAL DISEASE; MOOD; NONHUMAN; OLFACTORY BULBECTOMY; PREVALENCE; PRIORITY JOURNAL; SCHIZOPHRENIA; SMOKING; SOCIAL INTERACTION; STEREOTYPY; SUBSTANCE ABUSE; TASK PERFORMANCE; TOBACCO CONSUMPTION; TOBACCO DEPENDENCE; TRANSCRANIAL MAGNETIC STIMULATION; WORKING MEMORY; ANIMAL; DISEASE MODEL; DISEASE PREDISPOSITION;

ANIMALS; COMORBIDITY; DISEASE MODELS, ANIMAL; DISEASE SUSCEPTIBILITY; MENTAL DISORDERS; TOBACCO USE DISORDER;

EID: 84927522479     PISSN: 18663370     EISSN: 18663389     Source Type: Book Series    
DOI: 10.1007/978-3-319-13482-6_6     Document Type: Article

References (99)

1. Acri JB, Brown KJ, Saah MI, Grunberg NE (1995) Strain and age differences in acoustic startle responses and effects of nicotine in rats. Pharmacol Biochem Behav 50:191–198
2. Agrawal A, Budney AJ, Lynskey MT (2012) The co-occurring use and misuse of cannabis and tobacco: a review. Addiction 107:1221–1233
3. Andreasen JT, Redrobe JP (2009a) Antidepressant-like effects of nicotine and mecamylamine in the mouse forced swim and tail suspension tests: role of strain, test and sex. Behav Pharmacol20:286–295
4. Andreasen JT, Redrobe JP (2009b) Nicotine, but not mecamylamine, enhances antidepressant-like effects of citalopram and reboxetine in the mouse forced swim and tail suspension tests. Behav Brain Res 197:150–156
5. Andreasen JT, Olsen GM, Wiborg O, Redrobe JP (2009) Antidepressant-like effects of nicotinic acetylcholine receptor antagonists, but not agonists, in the mouse forced swim and mouse tail suspension tests. J Psychopharmacol 23:797–804
6. Andreasen JT, Henningsen K, Bate S, Christiansen S, Wiborg O (2011) Nicotine reverses anhedonic-like response and cognitive impairment in the rat chronic mild stress model of depression: comparison with sertraline. J Psychopharmacol 25:1134–1141
7. Balerio GN, Aso E, Maldonado R (2005) Involvement of the opioid system in the effects induced by nicotine on anxiety-like behaviour in mice. Psychopharmacology 181:260–269
8. Balerio GN, Aso E, Maldonado R (2006) Role of the cannabinoid system in the effects induced by nicotine on anxiety-like behaviour in mice. Psychopharmacology 184:504–513
9. Balsevich G, Poon A, Goldowitz D, Wilking Ja (2014) The effects of pre- and post-natal nicotine exposure and genetic background on the striatum and behavioral phenotypes in the mouse. Behav Brain Res 266:7–18
10. Battjes RJ (1988) Smoking as an issue in alcohol and drug abuse treatment. Addict Behav 13:225–230
11. Berg SA, Chambers RA (2008) Accentuated behavioral sensitization to nicotine in the neonatal ventral hippocampal lesion model of schizophrenia. Neuropharmacology 54:1201–1207
12. Berg SA, Sentir AM, Cooley BS, Engleman EA, Chambers RA (2014) Nicotine is more addictive, not more cognitively therapeutic in a neurodevelopmental model of schizophrenia produced by neonatal ventral hippocampal lesions. Addict Biol 19:1020–1031
13. Besson M, David V, Baudonnat M, Cazala P, Guilloux JP, Reperant C, Cloez-Tayarani I, Changeux JP, Gardier AM, Granon S (2012) Alpha7-nicotinic receptors modulate nicotine-induced reinforcement and extracellular dopamine outflow in the mesolimbic system in mice.Psychopharmacology 220:1–14
14. Bhattacharya SK, Chakrabarti A, Sandler M, Glover V (1995) Rat brain monoamine oxidase A and B inhibitory (tribulin) activity during drug withdrawal anxiety. Neurosci Lett 199:103–106
15. Biala G, Kruk M (2009) Effects of co-administration of bupropion and nicotine or D-amphetamine on the elevated plus maze test in mice. J Pharm Pharmacol 61:493–502
16. Biala G, Kruk M, Budzynska B (2009) Effects of the cannabinoid receptor ligands on anxiety-related effects of d-amphetamine and nicotine in the mouse elevated plus maze test. J Physiol Pharmacol 60:113–122
17. Braun Aa, Skelton MR, Vorhees CV, Williams MT (2011) Comparison of the elevated plus and elevated zero mazes in treated and untreated male Sprague-Dawley rats: effects of anxiolytic and anxiogenic agents. Pharmacol Biochem Behav 97:406–415
18. Brooner RK, King VL, Kidorf M, Schmidt CW Jr, Bigelow GE (1997) Psychiatric and substance use comorbidity among treatment-seeking opioid abusers. Arch Gen Psychiatry 54:71–80
19. Brown RW, Maple AM, Perna MK, Sheppard AB, Cope ZA, Kostrzewa RM (2012) Schizophrenia and substance abuse comorbidity: nicotine addiction and the neonatal quinpirole model. Dev Neurosci 34:140-151
20. Cope ZA, Huggins KN, Sheppard AB, Noel DM, Roane DS, Brown RW (2010) Neonatal quinpirole treatment enhances locomotor activation and dopamine release in the nucleus accumbens core in response to amphetamine treatment in adulthood. Synapse 64:289-300
21. Corrigall WA (1991) Understanding brain mechanisms in nicotine reinforcement. Br J Addict86:507-510
22. Curzon P, Kim DJ, Decker MW (1994) Effect of nicotine, lobeline, and mecamylamine on sensory gating in the rat. Pharmacol Biochem Behav 49:877-882
23. Dani JA, De Biasi M (2001) Cellular mechanisms of nicotine addiction. Pharmacol Biochem Behav 70:439–446
24. Elliott BM, Faraday MM, Phillips JM, Grunberg NE (2004) Effects of nicotine on elevated plus maze and locomotor activity in male and female adolescent and adult rats. Pharmacol Biochem Behav 77:21-28
25. Ericson M, Olausson P, Engel JA, Söderpalm B (2000) Nicotine induces disinhibitory behavior in the rat after subchronic peripheral nicotinic acetylcholine receptor blockade. Eur J Pharmacol397:103-111
26. Faraday MM, Rahman MA, Scheufele PM, Grunberg NE (1998) Nicotine administration impairs sensory gating in Long-Evans rats. Pharmacol Biochem Behav 61:281-289
27. Faraday MM, O’Donoghue VA, Grunberg NE (1999) Effects of nicotine and stress on startle amplitude and sensory gating depend on rat strain and sex. Pharmacol Biochem Behav 62:273-284
28. File SE, Kenny PJ, Ouagazzal AM (1998) Bimodal modulation by nicotine of anxiety in the social interaction test: role of the dorsal hippocampus. Behav Neurosci 112:1423-1429
29. File SE, Cheeta S, Kenny PJ (2000) Neurobiological mechanisms by which nicotine mediates different types of anxiety. Eur J Pharmacol 393:231-236
30. Fowler CD, Lu Q, Johnson PM, Marks MJ, Kenny PJ (2011) Habenular alpha5 nicotinic receptor subunit signalling controls nicotine intake. Nature 471:597-601
31. Fowler CD, Tuesta L, Kenny PJ (2013) Role of alpha5* nicotinic acetylcholine receptors in the effects of acute and chronic nicotine treatment on brain reward function in mice. Psychopharmacology 229:503-513
32. George SA, Moselhy H (2005) “Gateway hypothesis”—a preliminary evaluation of variables predicting non-conformity. Addict Disord Treat 4:39–40
33. Giros B, Jaber M, Jones SR, Wightman RM, Caron MG (1996) Hyperlocomotion and indifference to cocaine and amphetamine in mice lacking the dopamine transporter. Nature 379:606-612
34. Hien D, Zimberg S, Weisman S, First M, Ackerman S (1997) Dual diagnosis subtypes in urban substance abuse and mental health clinics. Psychiatr Serv 48:1058-1063
35. Irvine EE, Cheeta S, File SE (1999) Time-course of changes in the social interaction test of anxiety following acute and chronic administration of nicotine. Behav Pharmacol 10:691-697
36. Irvine EE, Bagnalasta M, Marcon C, Motta C, Tessari M, File SE, Chiamulera C (2000) Nicotine self-administration and withdrawal: modulation of anxiety in the social interaction test in rats. Psychopharmacology 153:315-320
37. Irvine EE, Cheeta S, File SE (2001) Tolerance to nicotine’s effects in the elevated plus-maze and increased anxiety during withdrawal. Pharmacol Biochem Behav 68:319-325
38. Kandel D (1975) Stages in adolescent involvement in drug use. Science 190:912-914 Kandel D, Faust R (1975) Sequence and stages in patterns of adolescent drug use. Arch Gen Psychiatry 32:923-932
39. Katz RJ (1982) Animal model of depression: pharmacological sensitivity of a hedonic deficit.Pharmacol Biochem Behav 16:965-968
40. Kayir H, Goktalay G, Yavuz O, Uzbay TI (2011) Impact of baseline prepulse inhibition on nicotine-induced locomotor sensitization in rats. Behav Brain Res 216:275-280
41. Kelsey JE, Calabro S (2008) Rimonabant blocks the expression but not the development of locomotor sensitization to nicotine in rats. Psychopharmacology 198:461–466
42. Kessler DA, Hass AE, Feiden KL, Lumpkin M, Temple R (1996a) Approvalof new drugsinthe United States. Comparison with the United Kingdom, Germany, and Japan. JAMA 276: 1826–1831
43. Kessler DA, Witt AM, Barnett PS, Zeller MR, Natanblut SL, Wilkenfeld JP, Lorraine CC, Thompson LJ, Schultz WB (1996b) The food and drug administration’s regulation of tobacco products. N Engl J Med 335:988–994
44. Kupferschmidt DA, Funk D, Erb S, Lê AD (2010) Age-related effects of acute nicotine on behavioural and neuronal measures of anxiety. Behav Brain Res 213:288–292
45. Laviolette SR, van der Kooy D (2004) The neurobiology of nicotine addiction: bridging the gap from molecules to behaviour. Nat Rev Neurosci 5:55–65
46. Le AD, Li Z, Funk D, Shram M, Li TK, Shaham Y (2006) Increased vulnerability to nicotine self-administration and relapse in alcohol-naive offspring of rats selectively bred for high alcohol intake. J Neurosci 26:1872–1879
47. Le AD, Lo S, Harding S, Juzytsch W, Marinelli PW, Funk D (2010) Coadministration of intravenous nicotine and oral alcohol in rats. Psychopharmacology 208:475–486
48. Levine A, Huang Y, Drisaldi B, Griffin EA, Jr, Pollak DD, Xu S, Yin D, Schaffran C, Kandel DB, Kandel ER (2011) Molecular mechanism for a gateway drug: epigenetic changes initiated by nicotine prime gene expression by cocaine. Sci Transl Med 3:107-109
49. Lev-Ran S, Imtiaz S, Rehm J, Le Foll B (2013) Exploring the association between lifetime prevalence of mental illness and transition from substance use to substance use disorders:results from the national epidemiologic survey of alcohol and related conditions (NESARC).Am J Addict 22:93–98
50. Lipska BK, Weinberger DR (2002) A neurodevelopmental model of schizophrenia: neonatal disconnection of the hippocampus. Neurotox Res 4:469–475
51. Lipska BK, Aultman JM, Verma A, Weinberger DR, Moghaddam B (2002) Neonatal damage of the ventral hippocampus impairs working memory in the rat. Neuropsychopharmacology 27:47–54
52. Marshall CE, Dadmarz M, Hofford JM, Gottheil E, Vogel WH (2003) Self-administration of both ethanol and nicotine in rats. Pharmacology 67:143–149
53. Matta SG, Elberger AJ (2007) Combined exposure to nicotine and ethanol throughout full gestation results in enhanced acquisition of nicotine self-administration in young adult rat offspring. Psychopharmacology 193:199–213
54. Mayet A, Legleye S, Chau N, Falissard B (2011) Transitions between tobacco and cannabis use among adolescents: a multi-state modeling of progression from onset to daily use. Addict Behav 36:1101–1105
55. Nestler EJ, Hyman SE (2010) Animal models of neuropsychiatric disorders. Nat Neurosci 13:1161–1169
56. Olausson P, Akesson P, Petersson A, Engel JA, Söderpalm B (2001) Behavioral and neurochemical consequences of repeated nicotine treatment in the serotonin-depleted rat. Psychopharmacology 155:348–361
57. Panlilio LV, Zanettini C, Barnes C, Solinas M, Goldberg SR (2013) Prior exposure to THC increases the addictive effects of nicotine in rats. Neuropsychopharmacology 38:1198–1208
58. Patton GC, Coffey C, Carlin JB, Sawyer SM, Lynskey M (2005) Reverse gateways? Frequent cannabis use as a predictor of tobacco initiation and nicotine dependence. Addiction 100:1518–1525
59. Pellow S, Chopin P, File SE, Briley M (1985) Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J Neurosci Methods 14:149–167
60. Perna MK, Cope ZA, Maple AM, Longacre ID, Correll JA, Brown RW (2008) Nicotine sensitization in adult male and female rats quinpirole-primed as neonates. Psychopharmacol-ogy 199:67–75
61. Peters EN, Budney AJ, Carroll KM (2012) Clinical correlates of co-occurring cannabis and tobacco use: a systematic review. Addiction 107:1404–1417
62. Picciotto MR, Corrigall WA (2002) Neuronal systems underlying behaviors related to nicotine addiction: neural circuits and molecular genetics. J Neurosci 22:3338–3341
63. 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
64. Pons S, Fattore L, Cossu G, Tolu S, Porcu E, McIntosh JM, Changeux JP, Maskos U, Fratta W (2008) Crucial role of alpha4 and alpha6 nicotinic acetylcholine receptor subunits from ventral tegmental area in systemic nicotine self-administration. J Neurosci 28:12318–12327
65. Porsolt RD, Bertin A, Jalfre M (1977) Behavioral despair in mice: a primary screening test for antidepressants. Arch Int Pharmacodyn Ther 229:327–336
66. Porsolt RD, Anton G, Blavet N, Jalfre M (1978) Behavioral despair in rats: a new model sensitive to antidepressant treatments. Eur J Pharmacol 47:379–391
67. Redner R, White TJ, Harder VS, Higgins ST (2014) Vulnerability to smokeless tobacco use among those dependent on alcohol or illicit drugs. Nicotine Tob Res 16:216–223
68. Regier DA, Farmer ME, Rae DS, Locke BZ, Keith SJ, Judd LL, Goodwin FK (1990) Comorbidity of mental disorders with alcohol and other drug abuse. Results from the epidemiologic catchment area (ECA) study. JAMA 264:2511–2518
69. Rodvelt KR, Bumgarner DM, Putnam WC, Miller DK (2007) WIN-55,212-2 and SR-141716A alter nicotine-induced changes in locomotor activity, but do not alter nicotine-evoked [3H] dopamine release. Life Sci 80:337–344
70. SAMHSA (2012) Results from the 2012 national survey on drug use and health: summary of national findings, SAMHSA,
71. Rockville Sams-Dodd F, Lipska BK, Weinberger DR (1997) Neonatal lesions of the rat ventral hippocampus result in hyperlocomotion and deficits in social behaviour in adulthood. Psychopharmacology132:303–310
72. antiago SE, Huffman KJ (2014) Prenatal nicotine exposure increases anxiety and modifies sensorimotor integration behaviors in adult female mice. Neurosci Res 79:41–51
73. Schreiber R, Dalmus M, De Vry J (2002) Effects of alpha 4/beta 2- and alpha 7-nicotine acetylcholine receptor agonists on prepulse inhibition of the acoustic startle response in rats and mice. Psychopharmacology 159:248–257
74. Semba J, Mataki C, Yamada S, Nankai M, Toru M (1998) Antidepressantlike effects of chronic nicotine on learned helplessness paradigm in rats. Biol Psychiatry 43:389–391
75. Slawecki CJ, Gilder A, Roth J, Ehlers CL (2003) Increased anxiety-like behavior in adult rats exposed to nicotine as adolescents. Pharmacol Biochem Behav 75:355–361
76. Slawecki CJ, Thorsell A, Ehlers CL (2004) Long-term neurobehavioral effects of alcohol or nicotine exposure in adolescent animal models. Ann NY Acad Sci 1021:448–452
77. Suemaru K, Yasuda K, Cui R, Li B, Umeda K (2006) Antidepressant-like action of nicotine in forced swimming test and brain serotonin in mice. Physiol Behav 88:545–549
78. Swendsen J, Conway KP, Degenhardt L, Glantz M, Jin R, Merikangas KR, Sampson N, Kessler RC (2010) Mental disorders as risk factors for substance use, abuse and dependence: results from the 10-year follow-up of the national comorbidity survey. Addiction 105:1117–1128
79. Szabo ST, Fowler JC, Froeliger B, Lee TH (2014) Time-dependent changes in nicotine behavioral responsivity during early withdrawal from chronic cocaine administration and attenuation of cocaine sensitization by mecamylamine. Behav Brain Res 262:42–46
80. Tapper AR, McKinney SL, Nashmi R, Schwarz J, Deshpande P, Labarca C, Whiteaker P, Marks MJ, Collins AC, Lester HA (2004) Nicotine activation of alpha4* receptors: sufficient for reward, tolerance, and sensitization. Science 306:1029–1032
81. Tarter RE, Vanyukov M, Kirisci L, Reynolds M, Clark DB (2006) Predictors of marijuana use in adolescents before and after licit drug use: examination of the gateway hypothesis. Am J psychiatry 163:2134–2140
82. Timberlake DS, Haberstick BC, Hopfer CJ, Bricker J, Sakai JT, Lessem JM, Hewitt JK (2007) Progression from marijuana use to daily smoking and nicotine dependence in a national sample of U.S. adolescents. Drug Alcohol Depend 88:272–281
83. Tizabi Y, Overstreet DH, Rezvani AH, Louis VA, Clark E, Janowsky DS, Kling MA (1999) Antidepressant effects of nicotine in an animal model of depression. Psychopharmacology 142:193–199
84. Tizabi Y, Getachew B, Rezvani AH, Hauser SR, Overstreet DH (2009) Antidepressant-like effects of nicotine and reduced nicotinic receptor binding in the Fawn-Hooded rat, an animal model of co-morbid depression and alcoholism. Prog Neuropsychopharmacol Biol Psychiatry 33:398–402
85. Tizabi Y, Hauser SR, Tyler KY, Getachew B, Madani R, Sharma Y, Manaye KF (2010) Effects of nicotine on depressive-like behavior and hippocampal volume of female WKY rats. Prog Neuropsychopharmacol Biol Psychiatry 34:62-69
86. Tullis LM, Dupont R, Frost-Pineda K, Gold MS (2003) Marijuana and tobacco: a major connection? J Addict Dis 22:51-62
87. Vanyukov MM, Tarter RE, Kirillova GP, Kirisci L, Reynolds MD, Kreek MJ, Conway KP, Maher BS, Iacono WG, Bierut L, Neale MC, Clark DB, Ridenour TA (2012) Common liability to addiction and “gateway hypothesis”: theoretical, empirical and evolutionary perspective. Drug Alcohol Depend 123:S3-S17
88. Varani AP, Moutinho LM, Bettler B, Balerio GN (2012) Acute behavioural responses to nicotine and nicotine withdrawal syndrome are modified in GABA(B1) knockout mice. Neuropharmacology 63:863-872
89. Vaughn M, Wallace J, Perron B, Copeland V, Howard M (2008) Does marijuana use serve as a gateway to cigarette use for high-risk African-American youth? Am J Drug Alcohol Abuse 34:782-791
90. Vázquez-Palacios G, Bonilla-Jaime H, Velázquez-Moctezuma J (2004) Antidepressant-like effects of the acute and chronic administration of nicotine in the rat forced swimming test and its interaction with fluoxetine [correction of flouxetine]. Pharmacol Biochem Behav 78:165-169
91. Vázquez-Palacios G, Bonilla-Jaime H, Velázquez-Moctezuma J (2005) Antidepressant effects of nicotine and fluoxetine in an animal model of depression induced by neonatal treatment with clomipramine. Prog Neuropsychopharmacol Biol Psychiatry 29:39–46
92. Vieyra-Reyes P, Mineur YS, Picciotto MR, Tiinez I, Vidaltamayo R, Drucker-Colín R (2008) Antidepressant-like effects of nicotine and transcranial magnetic stimulation in the olfactorybulbectomy rat model of depression. Brain Res Bull 77:13-18
93. Villégier A-S, Gallager B, Heston J, Belluzzi JD, Leslie FM (2010) Age influences the effects of nicotine and monoamine oxidase inhibition on mood-related behaviors in rats. Psychophar-macology 208:593-601
94. Wang T, Han W, Wang B, Jiang Q, Solberg-Woods LC, Palmer AA, Chen H (2014) Propensity for social interaction predicts nicotine-reinforced behaviors in outbred rats. Genes Brain Behav 13:202-212
95. Watkins SS, Koob GF, Markou A (2000) Neural mechanisms underlying nicotine addiction: acute positive reinforcement and withdrawal. Nicotine Tob Res 2:19-37
96. Weiss S, Nosten-Bertrand M, McIntosh JM, Giros B, Martres MP (2007) Nicotine improves cognitive deficits of dopamine transporter knockout mice without long-term tolerance.Neuropsychopharmacology 32:2465-2478
97. Yamaguchi K, Kandel DB (1984) Patterns of drug use from adolescence to young adulthood: II. Sequences of progression. Am J Public Health 74:668-672
98. Zarrindast MR, Aghamohammadi-Sereshki A, Rezayof A, Rostami P (2012) Nicotine-induced anxiogenic-like behaviours of rats in the elevated plus-maze: possible role of NMDA receptors of the central amygdala. J Psychopharmacol 26:555-563
99. Zickler P (2000) Nicotine craving and heavy smoking may contribute to increased use of cocaine and heroin. NIDA Notes 15