Threshold of adulthood for the onset of nicotine self-administration in male and female rats

Behavioural Brain Research

Volumn 225, Issue 2, 2011, Pages 473-481

  Levin, Edward D ^a   Slade, Susan ^a   Wells, Corinne ^a   Cauley, Marty ^a   Petro, Ann ^a   Vendittelli, Analise ^a   Johnson, Michael ^a   Williams, Paul ^a   Horton, Kofi ^a   Rezvani, Amir H ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Adolescence; Nicotine; Nicotinic; Self administration

Indexed keywords

COCAINE; NICOTINE;

ABSTINENCE; AGE DISTRIBUTION; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DRUG SEEKING BEHAVIOR; FEMALE; MALE; NONHUMAN; ONSET AGE; PERCEPTIVE THRESHOLD; PRIORITY JOURNAL; RAT; SEX DIFFERENCE; TOBACCO DEPENDENCE;

AGE FACTORS; ANIMALS; COCAINE; CONDITIONING, OPERANT; CRITICAL PERIOD (PSYCHOLOGY); ESTRUS; FEMALE; MALE; NICOTINE; RATS; RATS, SPRAGUE-DAWLEY; REINFORCEMENT SCHEDULE; SELF ADMINISTRATION; SEX CHARACTERISTICS;

EID: 80052969292     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2011.08.005     Document Type: Article

References (66)

1. Centers for Disease Control and Prevention Differences in the age of smoking initiation between blacks and whites, United States. Mortality and Morbidity Weekly Report 1991, 40:754-757.
2. Rigotti N. How can we help the remaining smokers to quit?. American Journal of Preventative Medicine 1990, 6:249-250.
3. Eissenberg T., Balster R.L. Initial tobacco use episodes in children and adolescents: current knowledge, future directions. Drug & Alcohol Dependence 2000, 59(Suppl. 1):S41-S60.
4. Glynn T., Greenwald P., Mills S., Manley M. Youth tobacco use in the United States: Problems, progress, goals, and potential solutions. Preventative Medicine 1993, 22:568-575.
5. US Public Health Service. Preventing tobacco use among young people: a report of the Surgeon General. US Department of Health, Education and Welfare. Washington, DC: US Government Printing Office; 1994.
6. Chassin L., Presson C.C., Rose J.S., Sherman S.J. The natural history of cigarette smoking from adolescence to adulthood: Demographic predictors of continuity and change. Health Psychology 1996, 15:478-484.
7. Pomerleau C., Pomerleau O. Characteristics of early- and late-onset smokers 2000, Society for Research on Nicotine and Tobacco, Arlington, VA.
8. Lloyd E., Niaura R., Kazura A. The progression of nicotine dependence in adolescents 2000, Society for Research on Nicotine and Tobacco, Arlington, VA.
9. Breslau N., Peterson E.L. Smoking cessation in young adults: age at initiation of cigarette smoking and other suspected influences. Am. J. Public Health 1996, 86:214-220.
10. Brownson R., DiLorenzo T., Van Tuinen M., Finger W. Patterns of cigarette and smokeless tobacco use among children and adolescents. Preventative Medicine 1991, 19:170-180.
11. Le Foll B., Gallo A., Le Strat Y., Lu L., Gorwood P. Genetics of dopamine receptors and drug addiction: a comprehensive review. Behavioural Pharmacology 2009, 20(1):1-17.
12. Spear L.P., Brake S.C. Periadolescence: Age-dependent behavior and psychopharmacological responsivity in rats. Develop. Psychobiol. 1983, 16:83-109.
13. Spear L.P. The adolescent brain and age-related behavioral manifestations. Neuroscience and Biobehavioral Reviews 2000, 24:417-463.
14. Shram M.J., Funk D., Li Z., Le A.D. Periadolescent and adult rats respond differently in tests measuring the rewarding and aversive effects of nicotine. Psychopharmacology 2006, 186(2):201-208.
15. Vastola B., Douglas L., Varlinskaya E., Spear L. Nicotine-induced conditioned place preference in adolescent and adult rats. Physiology & Behavior 2002, 77:107-114.
16. Belluzzi J., Lee A., Oliff H., Leslie F. Age-dependent effects of nicotine on locomotor activity and conditioned place preference in rats. Psychopharmacology 2004, 174:389-395.
17. Shram M.J., Le A.D. Adolescent male Wistar rats are more responsive than adult rats to the conditioned rewarding effects of intravenously administered nicotine in the place conditioning procedure. Behavioural Brain Research 2010, 206(2):240-244.
18. Nolley E.P., Kelley B.M. Adolescent reward system perseveration due to nicotine: studies with methylphenidate. Neurotoxicology & Teratology 2007, 29(1):47-56.
19. Kota D., Martin B.R., Damaj M.I. Age-dependent differences in nicotine reward and withdrawal in female mice. Psychopharmacology 2008, 198:201-210.
20. O'Dell L.E., Bruijnzeel A.W., Smith R.T., Parsons L.H., Merves M.L., Goldberger B.A., et al. Diminished nicotine withdrawal in adolescent rats: implications for vulnerability to addiction. Psychopharmacology 2006, 186(4):612-619.
21. O'Dell L.E., Bruijnzeel A.W., Ghozland S., Markou A., Koob G.F. Nicotine withdrawal in adolescent and adult rats. Annals of the New York Academy of Sciences 2004, 1021:167-174.
22. O'Dell L.E., Torres O.V., Natividad L.A., Tejeda H.A. Adolescent nicotine exposure produces less affective measures of withdrawal relative to adult nicotine exposure in male rats. Neurotoxicology & Teratology 2007, 29(1):17-22.
23. Slawecki C.J., Ehlers C.L. Lasting effects of adolescent nicotine exposure on the electroencephalogram, event related potentials, and locomotor activity in the rat. Brain Research Developmental Brain Research 2002, 138(1):15-25.
24. Slawecki C.J., Gilder A., Roth J., Ehlers C.L. Increased anxiety-like behavior in adult rats exposed to nicotine as adolescents. Pharmacology, Biochemistry & Behavior 2003, 75(2):355-361.
25. Rezvani A.H., Levin E.D. Adolescent and adult rats respond differently to nicotine and alcohol: motor activity and body temperature. International Journal of Developmental Neuroscience 2004, 22(5-6):349-354.
26. Brielmaier J.M., McDonald C.G., Smith R.F. Immediate and long-term behavioral effects of a single nicotine injection in adolescent and adult rats. Neurotoxicology & Teratology 2007, 29(1):74-80.
27. Laviola G., Macri S., Morley-Fletcher S., Adriani W. Risk-taking behavior in adolescent mice: psychobiological determinants and early epigenetic influence. Neuroscience & Biobehavioral Reviews 2003, 27(1-2):19-31.
28. Trauth J.A., Seidler F.J., McCook E.C., Slotkin T.A. Adolescent nicotine exposure causes persistent upregulation of nicotinic cholinergic receptors in rat brain regions. Brain Research 1999, 851(1-2):9-19.
29. Trauth J.A., McCook E.C., Seidler F.J., Slotkin T.A. Modeling adolescent nicotine exposure: Effects on cholinergic systems in rat brain regions. Brain Research 2000, 873(1):18-25.
30. Trauth J.A., Seidler F.J., Ali S.F., Slotkin T.A. Adolescent nicotine exposure produces immediate and long-term changes in CNS noradrenergic and dopaminergic function. Brain Research 2001, 892(2):269-280.
31. Abreu-Villaca Y., Seidler F.J., Qiao D., Tate C.A., Cousins M.M., Thillai I., et al. Short-term adolescent nicotine exposure has immediate and persistent effects on cholinergic systems: critical periods, patterns of exposure, dose thresholds. Neuropsychopharmacology 2003, 28(11):1935-1949.
32. Abreu-Villaca Y., Seidler F.J., Tate C.A., Slotkin T.A. Nicotine is a neurotoxin in the adolescent brain: critical periods, patterns of exposure, regional selectivity, and dose thresholds for macromolecular alterations. Brain Research 2003, 979(1-2):114-128.
33. Slotkin T.A. Nicotine and the adolescent brain: insights from an animal model. Neurotoxicology & Teratology 2002, 24(3):369-384.
34. Abreu-Villaca Y., Seidler F.J., Slotkin T.A. Impact of adolescent nicotine exposure on adenylyl cyclase-mediated cell signaling: enzyme induction, neurotransmitter-specific effects, regional selectivities, and the role of withdrawal. Brain Research 2003, 988(1-2):164-172.
35. Slotkin T.A., Ryde I.T., Tate C.A., Seidler F.J. Lasting effects of nicotine treatment and withdrawal on serotonergic systems and cell signaling in rat brain regions: separate or sequential exposure during fetal development and adulthood. Brain Research Bulletin 2007, 73(4-6):259-272.
36. Azam L., Chen Y., Leslie F.M. Developmental regulation of nicotinic acetylcholine receptors within midbrain dopamine neurons. Neuroscience 2007, 144(4):1347-1360.
37. Doura M.B., Gold A.B., Keller A.B., Perry D.C. Adult and periadolescent rats differ in expression of nicotinic cholinergic receptor subtypes and in the response of these subtypes to chronic nicotine exposure. Brain Reserch 2008, 1215:40-52.
38. Levin E.D., Rezvani A.H., Montoya D., Rose J.E., Swartzwelder H.S. Adolescent-onset nicotine self-administration modeled in female rats. Psychopharmacology 2003, 169:141-149.
39. Levin E.D., Lawrence S., Petro A., Horton K., Seidler F.J., Slotkin T.A. Increased nicotine self-administration following prenatal exposure in female rats. Pharmacology, Biochemistry and Behavior 2006, 85:669-674.
40. Levin E.D., Lawrence S., Petro A., Horton K., Rezvani A.H., Seidler F.J., et al. Adolescent vs. adult-onset nicotine self-administration in male rats: duration of effect and differential nicotinic receptor correlates. Neurotoxicology and Teratology 2007, 29:458-465.
41. Belluzzi J.D., Wang R., Leslie F.M. Acetaldehyde enhances acquisition of nicotine self-administration in adolescent rats. Neuropsychopharmacology 2005, 30(4):705-712.
42. Adriani W., Spijker S., Deroche-Gamonet V., Laviola G., Le Moal M., Smit A.B., et al. Evidence for enhanced neurobehavioral vulnerability to nicotine during periadolescence in rats. Journal of Neuroscience 2003, 23(11):4712-4716.
43. Klein L.C., Stine M.M., Vandenbergh D.J., Whetzel C.A., Kamens H.M. Sex differences in voluntary oral nicotine consumption by adolescent mice: a dose-response experiment. Pharmacology, Biochemistry & Behavior 2004, 78(1):13-25.
44. Chen H., Matta S.G., Sharp B.M. Acquisition of nicotine self-administration in adolescent rats given prolonged access to the drug. Neuropsychopharmacology 2007, 32(3):700-709.
45. Shram M.J., Li Z., Le A.D. Age differences in the spontaneous acquisition of nicotine self-administration in male Wistar and Long-Evans rats. Psychopharmacology 2008, 197(1):45-58.
46. Shram M.J., Funk D., Li Z., Le A.D. Nicotine self-administration, extinction responding and reinstatement in adolescent and adult male rats: evidence against a biological vulnerability to nicotine addiction during adolescence. Neuropsychopharmacology 2008, 33(4):739-748.
47. Chaudhri N., Caggiula A.R., Donny E.C., Booth S., Gharib M.A., Craven L.A., et al. Sex differences in the contribution of nicotine and nonpharmacological stimuli to nicotine self-administration in rats. Psychopharmacology 2005, 180(2):258-266.
48. Perkins K.A., Donny E., Caggiula A.R. Sex differences in nicotine effects and self-administration: review of human and animal evidence. Nicotine & Tobacco Research 1999, 1(4):301-315.
49. Rezvani A.H., Eddins D., Slade S., Hampton D.S., Christopher N.C., Petro A., et al. Neonatal 6-hydroxydopmine lesions of the frontal cortex in rats: Persisting effects on locomotor activity, learning and nicotine self-administration. Neuroscience 2008, 154:885-897.
50. Donny E.C., Caggiula A.R., Rowell P.P., Gharib M.A., Maldovan V., Booth S., et al. Nicotine self-administration in rats: estrous cycle effects, sex differences and nicotinic receptor binding. Psychopharmacology 2000, 151(4):392-405.
51. Lynch W.J. Sex and ovarian hormones influence vulnerability and motivation for nicotine during adolescence in rats. Pharmacology, Biochemistry & Behavior 2009, 94(1):43-50.
52. Feltenstein M.W., See R.E. Plasma progesterone levels and cocaine-seeking in freely cycling female rats across the estrous cycle. Drug & Alcohol Dependence 2007, 89(2-3):183-189.
53. Lynch W.J., Arizzi M.N., Carroll M.E. Effects of sex and the estrous cycle on regulation of intravenously self-administered cocaine in rats. Psychopharmacology 2000, 152(2):132-139.
54. Lynch W.J. Acquisition and maintenance of cocaine self-administration in adolescent rats: effects of sex and gonadal hormones. Psychopharmacology 2008, 197(2):237-246.
55. Roberts D.C., Bennett S.A., Vickers G.J. The estrous cycle affects cocaine self-administration on a progressive ratio schedule in rats. Psychopharmacology 1989, 98(3):408-411.
56. Feltenstein M.W., Byrd E.A., Henderson A.R., See R.E. Attenuation of cocaine-seeking by progesterone treatment in female rats. Psychoneuroendocrinology 2009, 34(3):343-352.
57. Cheeta S., Irvine E.E., Tucci S., Sandhu J., File S.E. In adolescence, female rats are more sensitive to the anxiolytic effect of nicotine than are male rats. Neuropsychopharmacology 2001, 25(4):601-607.
58. Collins S.L., Montano R., Izenwasser S. Nicotine treatment produces persistent increases in amphetamine-stimulated locomotor activity in periadolescent male but not female or adult male rats. Brain Research Developmental Brain Research 2004, 153(2):175-187.
59. Polesskaya O.O., Fryxell K.J., Merchant A.D., Locklear L.L., Ker K.F., McDonald C.G., et al. Nicotine causes age-dependent changes in gene expression in the adolescent female rat brain. Neurotoxicology & Teratology 2007, 29(1):126-140.
60. Elliott B.M., Faraday M.M., Phillips J.M., Grunberg N.E. Adolescent and adult female rats differ in sensitivity to nicotine's activity effects. Pharmacology, Biochemistry & Behavior 2005, 80(4):567-575.
61. Lynch W.J., Sofuoglu M. Role of progesterone in nicotine addiction: evidence from initiation to relapse. Experimental & Clinical Psychopharmacology 2010, 18(6):451-461.
62. Fone K.C., Porkess M.V. Behavioural and neurochemical effects of post-weaning social isolation in rodents-relevance to developmental neuropsychiatric disorders. Neuroscience and Biobehavioral Reviews 2008, 32:1087-1102.
63. Weintraub A., Singaravelu J., Bhatnagar S. Enduring and sex-specific effects of adolescent social isolation in rats on adult stress reactivity. Brain Research 2010, 1343:83-92.
64. Centers for Disease Control and Prevention Selected cigarette smoking initiation and quitting behaviors among high school students-United States, 1997. Mortality and Morbidity Weekly Report 1998, 47:386.
65. McQuown S.C., Belluzzi J.D., Leslie F.M. Low dose nicotine treatment during early adolescence increases subsequent cocaine reward. Neurotoxicology & Teratology 2007, 29(1):66-73.
66. Dao J.M., McQuown S.C., Loughlin S.E., Belluzzi J.D., Leslie F.M. Nicotine alters limbic function in adolescent rat by a 5-HT1A receptor mechanism. Neuropsychopharmacology 2011, 36:1-13.