Chronic ethanol exposure during adolescence alters the behavioral responsiveness to ethanol in adult mice

[en] Alcohol exposure during early adolescence is believed to durably alter the behavioral properties of ethanol, increasing the likelihood of later alcohol-related disorders. The aim of the present experiments was to characterize changes in the behavioral effects of ethanol in adult female Swiss mice after a chronic ethanol exposure during adolescence, extending from postnatal day 28 to postnatal day 42. After a chronic ethanol exposure during adolescence (daily injections of 0, 2.5 or 4 g/kg ethanol for 14 consecutive days), adult mice were tested at postnatal day 63. The locomotor stimulant effects of ethanol, together with ethanol sensitization were tested in experiment 1. In experiment 2, the sedative effects of ethanol were assessed with the loss of righting reflex procedure. Finally, in experiment 3, the anxiolytic effects of ethanol were tested with the light/dark box test. Adult mice chronically exposed to ethanol during adolescence showed a lower basal locomotor activity, but higher locomotor stimulant effects of ethanol than non-exposed mice. Additionally, these adult mice developed higher rates of ethanol sensitization after chronic re-exposure to ethanol in adulthood. Adult mice exposed to ethanol during adolescence also had a stronger tolerance to the sedative effects of high ethanol doses, although they showed no evidence of changes in the anxiolytic effects of ethanol. These results are in agreement with the thesis that chronic alcohol consumption during adolescence, especially in high amounts, increases the risk of later alcohol-related disorders.

Research center :

Centre de Neurosciences Cognitives et Comportementales - ULiège

Disciplines :

Neurosciences & behavior

Author, co-author :

Quoilin, Caroline ; Université de Liège - ULiège > Département de Psychologie : cognition et comportement > Psychologie quantitative

Didone, Vincent ; Université de Liège - ULiège > Département de Psychologie : cognition et comportement > Psychologie quantitative

Tirelli, Ezio ; Université de Liège - ULiège > Département de Psychologie : cognition et comportement > Neuroscience comportementale et psychopharmacologie expér.

Quertemont, Etienne ; Université de Liège - ULiège > Département de Psychologie : cognition et comportement > Psychologie quantitative

Language :

English

Title :

Chronic ethanol exposure during adolescence alters the behavioral responsiveness to ethanol in adult mice

Publication date :

2012

Journal title :

Behavioural Brain Research

ISSN :

0166-4328

eISSN :

1872-7549

Publisher :

Elsevier Science, Amsterdam, Netherlands

Volume :

229

Pages :

1-9

Peer reviewed :

Peer Reviewed verified by ORBi

Funders :

F.R.S.-FNRS - Fonds de la Recherche Scientifique [BE]

Available on ORBi :

since 17 January 2012

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Bibliography

Spear L.P. The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav 2000, 24:417-463.
Kandel D., Yamaguchi K. From beer to crack: developmental patterns of drug involvement. Am J Public Health 1993, 83:851-855.
Martin C.A., Kelly T.H., Rayens M.K., Brogli B.R., Brenzel A., Smith W.J., et al. Sensation seeking, puberty, and nicotine, alcohol, and marijuana use in adolescence. J Am Acad Child Adolesc Psychiatry 2002, 41:1495-1502.
Miller J.W., Naimi T.S., Brewer R.D., Jones S.E. Binge drinking and associated health risk behaviors among high school students. Pediatrics 2007, 119:76-85.
Substance Abuse and Mental Health Services Administration. Results from the 2009 National Survey on Drug Use and Health, vol. I. Summary of National Findings (Office of Applied Studies, NSDUH Series H-38A, HHS Publication No. SMA 10-4586Findings). Rockville, MD; 2010.
Bates M.E., Labouvie E.W. Adolescent risk factors and the prediction of persistent alcohol and drug use into adulthood. Alcohol Clin Exp Res 1995, 21:944-950.
Nelson D.E., Naimi T.S., Brewer R.D., Nelson H.A. State alcohol-use estimates among youth and adults, 1993-2005. Am J Prev Med 2009, 36:218-224.
Brunell C.S., Spear L.P. Effect of stress on the voluntary intake of a sweetened ethanol solution in pair-housed adolescent and adult rats. Alcohol Clin Exp Res 2005, 29:1641-1653.
Doremus T.L., Brunell S.C., Rajendran P., Spear L.P. Factors influencing elevated ethanol consumption in adolescent relative to adult rats. Alcohol Clin Exp Res 2005, 29:1796-1808.
Moore E.M., Mariani J.N., Linsenbardt D.N., Melón L.C., Boehm S.L Adolescent C57BL/6J (but not DBA/2J) mice consume greater amounts of limited-access ethanol compared to adults and display continued elevated ethanol intake into adulthood. Alcohol Clin Exp Res 2010, 34:734-742.
Vetter C.S., Doremus-Fitzwater T.L., Spear L.P. Time course of elevated ethanol intake in adolescent relative to adult rats under continuous, voluntary-access conditions. Alcohol Clin Exp Res 2007, 31:1159-1168.
Anthony J.C., Petronis K.R. Early-onset drug use and risk of later drug problems. Drug Alcohol Depend 1995, 40:9-15.
Robins L.N., Przybeck T.R. Age of onset of drug use as a factor in drug and other disorders. Etiology of drug abuse: implications for prevention 1985, 178-192. National Institute on Drug Abuse, Rockville, MD. C.L. Jones, R.L. Battjes (Eds.).
DeWit D.J., Adlaf E.M., Offord D.R., Ogborne A.C. Age at first alcohol use: a risk factor for the development of alcohol disorders. Am J Psychiatry 2000, 157:745-750.
Grant B.F., Dawson D.A. Age at onset of alcohol use and its association with DSM-IV alcohol abuse and dependence: results from the national longitudinal alcohol epidemiologic survey. J Subst Abuse 1997, 9:103-110.
Acevedo M.B., Molina J.C., Nizhnikov M.E., Spear N.E., Pautassi R.M. High ethanol dose during early adolescence induces locomotor activation and increases subsequent ethanol intake during late adolescence. Dev Psychobiol 2010, 52:424-440.
Bell R.L., Rodd Z.A., Sable H.J., Schultz J.A., Hsu C.C., Lumeng L., et al. Daily patterns of ethanol drinking in peri-adolescent and adult alcohol-preferring (P) rats. Pharmacol Biochem Behav 2006, 83:35-46.
Blizard D.A., Vandenbergh D.J., Jefferson A.L., Chatlos C.D., Vogler G.P., McClearn G.E. Effects of periadolescent ethanol exposure on alcohol preference in two BALB substrains. Alcohol 2004, 34:177-185.
Maldonado-Devincci A.M., Alipour K.K., Michael L.A., Kirstein C.L. Repeated binge ethanol administration during adolescence enhances voluntary sweetened ethanol intake in young adulthood in male and female rats. Pharmacol Biochem Behav 2010, 96:476-487.
Crews F., He J., Hodge C. Adolescent cortical development: a critical period of vulnerability for addiction. Pharmacol Biochem Behav 2007, 86:189-199.
Ernst M., Romeo R.D., Andersen S.L. Neurobiology of the development of motivated behaviors in adolescence: a window into a neural systems model. Pharmacol Biochem 2009, 93:199-211.
Giedd J.N. The teen brain: insights from neuroimaging. J. Adolesc Health 2008, 42:335-343.
Guerri C., Pascual M. Mechanisms involved in the neurotoxic, cognitive, and neurobehavioral effects of alcohol consumption during adolescence. Alcohol 2010, 44:15-26.
Brown S.A., Tapert S.F. Adolescence and the trajectory of alcohol use: basic to clinical studies. Ann N Y Acad Sci 2004, 1021:234-244.
Hanson K.L., Medina K.L., Padula C.B., Tapert S.F., Brown S.A. Impact of adolescent alcohol and drug use on neuropsychological functioning in young adulthood: 10-year outcomes. J Child Adolesc Subst Abuse 2011, 20:135-154.
Badanich K.A., Maldonado A.M., Kirstein C.L. Chronic ethanol exposure during adolescence increases basal dopamine in the nucleus accumbens septi during adulthood. Alcohol Clin Exp Res 2007, 31:895-900.
Coleman L.G., He J., Lee J., Styner M., Crews F.T. Adolescent binge drinking alters adult brain neurotransmitter gene expression, behavior, brain regional volumes, and neurochemistry in mice. Alcohol Clin Exp Res 2011, 35:671-688.
Maldonado-Devincci A.M., Badanich K.A., Kirstein C.L. Alcohol during adolescence selectively alters immediate and long-term behavior and neurochemistry. Alcohol 2010, 44:57-66.
Pascual M., Blanco A.M., Cauli O., Miñarro J., Guerri C. Intermittent ethanol exposure induces inflammatory brain damage and causes long-term behavioural alterations in adolescent rats. Eur J Neurosci 2007, 25:541-550.
Pascual M., Boix J., Felipo V., Guerri C. Repeated alcohol administration during adolescence causes changes in the mesolimbic dopaminergic and glutamatergic systems and promotes alcohol intake in the adult rat. J Neurochem 2009, 108:920-931.
Slawecki C.J., Betancourt M., Cole M., Ehlers C.L. Periadolescent alcohol exposure has lasting effects on adult neurophysiological function in rats. Dev Brain Res 2001, 128:63-72.
McBride W.J., Bell R.L., Rodd Z.A., Strother W.N., Murphy J.M. Adolescent alcohol drinking and its long-range consequences. Studies with animal models. Recent Dev Alcohol 2005, 17:123-142.
Diaz-Granados J.L., Graham D.L. The effects of continuous and intermittent ethanol exposure in adolesence on the aversive properties of ethanol during adulthood. Alcohol Clin Exp Res 2007, 31:2020-2027.
White A.M., Bae J.G., Truesdale M.C., Ahmad S., Wilson W.A., Swartzwelder H.S. Chronic-intermittent ethanol exposure during adolescence prevents normal developmental changes in sensitivity to ethanol-induced motor impairments. Alcohol Clin Exp Res 2002, 26:960-968.
White A.M., Ghia A.J., Levin E.D., Swartzwelder H.S. Binge pattern ethanol exposure in adolescent and adult rats: differential impact on subsequent responsiveness to ethanol. Alcohol Clin Exp Res 2000, 24:1251-1256.
Schulteis G., Archer C., Tapert S.F., Frank L.R. Intermittent binge alcohol exposure during the periadolescent period induces spatial working memory deficits in young adult rats. Alcohol 2008, 42:459-467.
Matthews D.B., Tinsley K.L., Diaz-Granados J.L., Tokunaga S., Silvers J.M. Chronic intermittent exposure to ethanol during adolescence produces tolerance to the hypnotic effects of ethanol in male rats: a dose-dependent analysis. Alcohol 2008, 42:617-621.
Silvers J.M., Tokunaga S., Mittleman G., Matthews D.B. Chronic intermittent injections of high-dose ethanol during adolescence produce metabolic, hypnotic, and cognitive tolerance in rats. Alcohol Clin Exp Res 2003, 27:1606-1612.
Wise R.A., Bozarth M.A. A psychomotor stimulant theory of addiction. Psychol Rev 1987, 94:469-492.
Robinson T.E., Berridge K.C. The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Res Rev 1993, 18:247-291.
Robinson T.E., Berridge K.C. Incentive-sensitization and addiction. Addiction 2001, 96:103-114.
Robinson T.E., Berridge K.C. Addiction. Annu Rev Psychol 2003, 54:25-53.
Koob G.F. The neurobiology of addiction: a neuroadaptational view relevant for diagnosis. Addiction 2006, 101:23-30.
Spanagel R., Montkowski A., Allingham K., Stöhr T., Shoaib M., Holsboer F., et al. Anxiety: a potential predictor of vulnerability to the initiation of ethanol self-administration in rats. Psychopharmacology 1995, 122:369-373.
Cappell H., Herman C.P. Alcohol and tension reduction. A review. Q J Stud Alcohol 1972, 33:33-64.
Schuckit M.A., Smith T.L., Kalmijn J., Tsuang J., Hesselbrock V., Bucholz K. Response to alcohol in daughters of alcoholics: a pilot study and a comparison with sons of alcoholics. Alcohol Alcohol 2000, 35:242-248.
Tirelli E., Laviola G., Adriani W. Ontogenesis of behavioral sensitization and conditioned place preference induced by psychostimulants in laboratory rodents. Neurosci Biobehav Rev 2003, 27:163-178.
Quoilin C, Didone V, Tirelli E, Quertemont E. Developmental differences in ethanol-induced sensitization using postweanling, adolescent, and adult Swiss mice. Psychopharmacology; in press.
Quoilin C., Didone V., Tirelli E., Quertemont E. Ontogeny of the stimulant and sedative effects of ethanol in male and female Swiss mice: gradual changes from weaning to adulthood. Psychopharmacology 2010, 212:501-512.
King T.S., Chinchilli V.M. Robust estimators of the concordance correlation coefficient. J Biopharm Stat 2001, 11:83-105.
Linsenbardt D.N., Moore E.M., Gross C.D., Goldfarb K.J., Blackman L.C., Boehm S.L. Sensitivity and tolerance to the hypnotic and ataxic effects of ethanol in adolescent and adult C57BL/6J and DBA/2J mice. Alcohol Clin Exp Res 2009, 33:464-476.
Stansfield K.H., Kirstein C.L. Chronic cocaine or ethanol exposure during adolescence alters novelty-related behaviors in adulthood. Pharmacol Biochem Behav 2007, 86:637-642.
Didone V., Quoilin C., Tirelli E., Quertemont E. Parametric analysis of the development and expression of ethanol-induced behavioral sensitization in female Swiss mice: effects of dose, injection schedule, and test context. Psychopharmacology 2008, 201:249-260.
Tambour S., Didone V., Tirelli E., Quertemont E. Locomotor effects of ethanol and acetaldehyde after peripheral and intraventricular injections in Swiss and C57BL/6J mice. Behav Brain Res 2006, 172:145-154.
Agabio R., Carai M.A., Lobina C., Pani M., Reali R., Vacca G., et al. Alcohol stimulates motor activity in selectively bred Sardinian alcohol-preferring (sP), but not in Sardinian alcohol-nonpreferring (sNP), rats. Alcohol 2001, 23:123-126.
Colombo G., Agabio R., Lobina C., Reali R., Vacca G., Gessa G.L. Stimulation of locomotor activity by voluntarily consumed ethanol in Sardinian alcohol-preferring rats. Eur J Pharmacol 1998, 357:109-113.
Rodd Z.A., Bell R.L., McKinzie D.L., Webster A.A., Murphy J.M., Lumeng L., et al. Low-dose stimulatory effects of ethanol during adolescence in rat lines selectively bred for high alcohol intake. Alcohol Clin Exp Res 2004, 28:535-543.
King A.C., Houle T., de Wit H., Holdstock L., Schuster A. Biphasic alcohol response differs in heavy versus light drinkers. Alcohol Clin Exp Res 2002, 26:827-835.
Leigh B.C. Beliefs about the effects of alcohol on self and others. J Stud Alcohol 1987, 48:467-475.
Schöberl S., Nickel P., Schmutzer G., Siekmeyer W., Kiess W. Acute ethanol intoxication among children and adolescents. A retrospective analysis of 173 patients admitted to a university children hospital. Klin Padiatr 2008, 220:253-258.
Lessov C.N., Phillips T.J. Duration of sensitization to the locomotor stimulant effects of ethanol in mice. Psychopharmacology 1998, 135:374-382.
Phillips T.J., Huson M., Gwiazdon C., Burkhart-Kasch S., Shen E.H. Effects of acute and repeated ethanol exposures on the locomotor activity of BXD recombinant inbred mice. Alcohol Clin Exp Res 1995, 19:269-278.
Benes F.M., Taylor J.B., Cunningham M.C. Convergence and plasticity of monoaminergic systems in the medial prefrontal cortex during the postnatal period: implications for the development of psychopathology. Cereb Cortex 2000, 10:1014-1027.
Stanwood G.D., McElligot S., Lu L., McGonigle P. Ontogeny of dopamine D3 receptors in the nucleus accumbens of the rat. Neurosci Lett 1997, 223:13-16.
Tarazi F.I., Baldessarini R.J. Comparative postnatal development of dopamine D(1), D(2) and D(4) receptors in rat forebrain. Int J Dev Neurosci 2000, 18:29-37.
Tarazi F.I., Tomasini E.C., Baldessarini R.J. Postnatal development of dopamine and serotonin transporters in rat caudate-putamen and nucleus accumbens septi. Neurosci Lett 1998, 254:21-24.
Doremus-Fitzwater T.L., Varlinskaya E.I., Spear L.P. Motivational systems in adolescence: possible implications for age differences in substance abuse and other risk-taking behaviors. Brain Cogn 2010, 72:114-123.
Insel T.R., Miller L.P., Gelhard R.E. The ontogeny of excitatory amino acid receptors in rat forebrain- N-methyl-d-aspartate and quisqualate receptors. Neuroscience 1990, 35:31-43.
Laurie D.J., Wisden W., Seeburg P.H. The distribution of thirteen GABA A receptor subunit mRNAs in the rat brain. III. Embryonic and postnatal development. J Neurosci 1992, 12:4151-4172.
Xia Y., Haddad G.G. Ontogeny and distribution of GABA A receptors in rat brainstem and rostral brain regions. Neuroscience 1992, 49:973-989.
Imperato A., Di Chiara G. Preferential stimulation of dopamine release in the nucleus accumbens of freely moving rats by ethanol. J Pharmacol Exp Ther 1986, 239:219-228.
Krystal J.H., Petrakis I.L., Mason G., Trevisan L., D'Souza D.C. N-methyl-d-aspartate glutamate receptors and alcoholism: reward, dependence, treatment, and vulnerability. Pharmacol Ther 2003, 99:79-94.
Martz A., Deitrich R.A., Harris R.A. Behavioral evidence for the involvement of gamma-aminobutyric acid in the actions of ethanol. Eur J Pharmacol 1983, 89:53-62.
Silveri M.M., Spear L.P. The effects of NMDA and GABA A pharmacological manipulations on ethanol sensitivity in immature and mature animals. Alcohol Clin Exp Res 2002, 26:449-456.
Sahr A.E., Thielen R.J., Lumeng L., Li T.K., McBride W.J. Long-lasting alterations of the mesolimbic dopamine system after periadolescent ethanol drinking by alcohol-preferring rats. Alcohol Clin Exp Res 2004, 28:702-711.
Devaud L.L., Smith F.D., Grayson D.R., Morrow A.L. Chronic ethanol consumption differentially alters the expression of gamma-aminobutyric acidA receptor subunit mRNAs in rat cerebral cortex: competitive, quantitative reverse transcriptase-polymerase chain reaction analysis. Mol Pharmacol 1995, 48:861-868.
Devaud L.L., Fritschy J.M., Sieghart W., Morrow A.L. Bidirectional alterations of GABA(A) receptor subunit peptide levels in rat cortex during chronic ethanol consumption and withdrawal. J Neurochem 1997, 69:126-130.
Matthews D.B., Devaud L.L., Fritschy J.M., Sieghart W., Morrow A.L. Differential regulation of GABA(A) receptor gene expression by ethanol in the rat hippocampus versus cerebral cortex. J Neurochem 1998, 70:1160-1166.