Abstract
Rationale
Vulnerability to alcoholism is determined by many factors, including the balance of pleasurable vs. aversive alcohol-induced sensations: pleasurable sensations increase intake, while aversive sensations decrease it. Female sex and adolescent age are associated with lower sensitivity to intake-reducing effects and more rapid development of alcohol abuse.
Objectives
This study assessed voluntary drinking and the aversive effects of alcohol to determine whether these measures are inversely related across the sexes and development.
Methods
Voluntary drinking of 20 % ethanol in an every-other-day (EOD) availability pattern and the dose–response relationship of ethanol conditioned taste aversion (CTA) were assessed in male and female adolescent and adult rats.
Results
CTA was sex specific in adult but not adolescent rats, with adult females exhibiting less aversion. Voluntary ethanol consumption varied according to age and individual differences but was not sex specific. Adolescents initially drank more than adults, exhibited greater day-to-day variation in consumption, were more susceptible to the alcohol deprivation effect, and took longer to establish individual differences in consumption patterns.
Conclusions
These results show that the emergence of intake patterns differs between adolescents and adults. Adolescents as a group initiate drinking at high levels but decrease intake as they mature. A subset of adolescents maintained high drinking levels into adulthood. In contrast, most adults consumed at steady, low levels, but a small subset quickly established and maintained high-consumption patterns. Adolescents also showed marked deprivation-induced increases. Sex differences were not observed in EOD drinking during either adolescence or adulthood.
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References
Becker HC, Anton RF, De Trana C, Randall CL (1985) Sensitivity to ethanol in female mice: effects of ovariectomy and strain. Life Sci 37:1293–300
Bell RL, Rodd ZA, Hsu CC, Lumeng L, Li TK, Murphy JM, McBride WJ (2004) Effects of concurrent access to a single concentration or multiple concentrations of ethanol on ethanol intake by periadolescent high-alcohol-drinking rats. Alcohol 33:107–15
Brunetti G, Carai MA, Lobina C, Melis S, Serra S, Vacca G, Gessa GL, Colombo G (2002) Differences in ethanol-induced conditioned taste aversion in Sardinian alcohol-preferring and Sardinian alcohol-nonpreferring rats. Alcohol 26:167–72
Busse GD, Freeman KB, Riley AL (2005) The interaction of sex and route of drug administration in cocaine-induced conditioned taste aversions. Pharmacol Biochem Behav 81:814–20
Cailhol S, Mormede P (2002) Conditioned taste aversion and alcohol drinking: strain and gender differences. J Stud Alcohol 63:91–9
Cason AM, Denbleyker M, Ferrence K, Smith JC, Houpt TA (2006) Sex and estrous cycle differences in the behavioral effects of high-strength static magnetic fields: role of ovarian steroids. Am J Physiol Regul Integr Comp Physiol 290:R659–67
Chambers KC, Sengstake CB (1976) Sexually dimorphic extinction of a conditioned taste aversion in rats. Animal learning & behavior 4:181–5
Chambers KC, Sengstake CB, Yoder RL, Thornton JE (1981) Sexually dimorphic acquisition of a conditioned taste aversion in rats: effects of gonadectomy, testosterone replacement and water deprivation. Physiol Behav 27:83–8
Chen K, Kandel DB (1995) The natural history of drug use from adolescence to the mid-thirties in a general population sample. Am J Public Health 85:41–7
Choleris E, Thomas AW, Ossenkopp K, Kavaliers M, Valsecchi P, Prato FS (2000) Sex differences in conditioned taste aversion and in the effects of exposure to a specific pulsed magnetic field in deer mice Peromyscus maniculatus. Physiol Behav 71:237–49
Daoura L, Haaker J, Nylander I (2011) Early environmental factors differentially affect voluntary ethanol consumption in adolescent and adult male rats. Alcohol Clin Exp Res 35:506–15
Doremus-Fitzwater TL, Spear LP (2007) Developmental differences in acute ethanol withdrawal in adolescent and adult rats. Alcohol Clin Exp Res 31:1516–27
Doremus TL, Brunell SC, Varlinskaya EI, Spear LP (2003) Anxiogenic effects during withdrawal from acute ethanol in adolescent and adult rats. Pharmacol Biochem Behav 75:411–8
El-Mas MM, Abdel-Rahman AA (2000) Ovariectomy alters the chronic hemodynamic and sympathetic effects of ethanol in radiotelemetered female rats. Clin Exp Hypertens 22:109–26
Ford MM, Eldridge JC, Samson HH (2002) Ethanol consumption in the female Long-Evans rat: a modulatory role of estradiol. Alcohol 26:103–13
Foy MR, Foy JG (2003) Reversal of long-delay conditioned taste aversion learning in rats by sex hormone manipulation. Integr Physiol Behav Sci 38:203–13
Froehlich JC, Harts J, Lumeng L, Li TK (1988) Differences in response to the aversive properties of ethanol in rats selectively bred for oral ethanol preference. Pharmacol Biochem Behav 31:215–22
Fullgrabe MW, Vengeliene V, Spanagel R (2007) Influence of age at drinking onset on the alcohol deprivation effect and stress-induced drinking in female rats. Pharmacol Biochem Behav 86:320–6
Green AS, Grahame NJ (2008) Ethanol drinking in rodents: is free-choice drinking related to the reinforcing effects of ethanol? Alcohol 42:1–11
Hilakivi-Clarke L (1996) Role of estradiol in alcohol intake and alcohol-related behaviors. J Stud Alcohol 57:162–70
Holstein SE, Spanos M, Hodge CW (2011) Adolescent C57BL/6J mice show elevated alcohol intake, but reduced taste aversion, as compared to adult mice: a potential behavioral mechanism for binge drinking. Alcohol Clin Exp Res 35:1842–51
Hwa LS, Chu A, Levinson SA, Kayyali TM, DeBold JF, Miczek KA (2011) Persistent escalation of alcohol drinking in C57BL/6J mice with intermittent access to 20 % ethanol. Alcohol Clin Exp Res 35:1938–47
Infurna RN, Spear LP (1979) Developmental changes in amphetamine-induced taste aversions. Pharmacol Biochem Behav 11:31–5
Li J, Zou Y, Ye JH (2011) Low frequency electroacupuncture selectively decreases voluntarily ethanol intake in rats. Brain Res Bull 86:428–34
Li TK, Lumeng L (1984) Alcohol preference and voluntary alcohol intakes of inbred rat strains and the National Institutes of Health heterogeneous stock of rats. Alcohol Clin Exp Res 8:485–6
Little PJ, Kuhn CM, Wilson WA, Swartzwelder HS (1996) Differential effects of ethanol in adolescent and adult rats. Alcohol Clin Exp Res 20:1346–51
Long J, Evans H (1922) The oestrous cycle in the rat and its associated phenomena. University of California Press, Berkeley
Lucas LA, McMillen BA (2002) Conditioned taste aversion and the Myers' high-ethanol-preferring rat. Alcohol Alcohol 37:427–31
Randall-Thompson JF, Riley AL (2003) Morphine-induced conditioned taste aversions: assessment of sexual dimorphism. Pharmacol Biochem Behav 76:373–81
Randall CL, Roberts JS, Del Boca FK, Carroll KM, Connors GJ, Mattson ME (1999) Telescoping of landmark events associated with drinking: a gender comparison. J Stud Alcohol 60:252–60
Rhodes JS, Ford MM, Yu CH, Brown LL, Finn DA, Garland T Jr, Crabbe JC (2007) Mouse inbred strain differences in ethanol drinking to intoxication. Genes Brain Behav 6:1–18
Rinker JA, Busse GD, Riley AL (2008) An assessment of sex differences in nicotine-induced conditioned taste aversions. Pharmacol Biochem Behav 88:427–31
Ristuccia RC, Spear LP (2005) Sensitivity and tolerance to autonomic effects of ethanol in adolescent and adult rats during repeated vapor inhalation sessions. Alcohol Clin Exp Res 29:1809–20
Robins LN, Przybeck TR (1985) Age of onset of drug use as a factor in drug and other disorders. NIDA Res Monogr 56:178–92
Rodd ZA, Bell RL, Sable HJ, Murphy JM, McBride WJ (2004) Recent advances in animal models of alcohol craving and relapse. Pharmacol Biochem Behav 79:439–50
Roma PG, Chen SA, Barr CS, Riley AL (2007) Dissociation between the aversive and pharmacokinetic effects of ethanol in female Fischer and Lewis rats. Behav Brain Res 182:51–6
Roma PG, Davis CM, Kohut SJ, Huntsberry ME, Riley AL (2008) Early maternal separation and sex differences in the aversive effects of amphetamine in adult rats. Physiol Behav 93:897–904
Roma PG, Flint WW, Higley JD, Riley AL (2006) Assessment of the aversive and rewarding effects of alcohol in Fischer and Lewis rats. Psychopharmacology (Berl) 189:187–99
Sabino V, Kwak J, Rice KC, Cottone P (2013) Pharmacological characterization of the 20 % alcohol intermittent access model in Sardinian alcohol-preferring rats: a model of binge-like drinking. Alcohol Clin Exp Res 37:635–43
Schramm-Sapyta NL, Cha YM, Chaudhry S, Wilson WA, Swartzwelder HS, Kuhn CM (2007) Differential anxiogenic, aversive, and locomotor effects of THC in adolescent and adult rats. Psychopharmacology (Berl) 191:867–77
Schramm-Sapyta NL, Difeliceantonio AG, Foscue E, Glowacz S, Haseeb N, Wang N, Zhou C, Kuhn CM (2010) Aversive Effects of Ethanol in Adolescent Versus Adult Rats: Potential Causes and Implication for Future Drinking. Alcohol Clin Exp Res
Schramm-Sapyta NL, Kingsley MA, Rezvani AH, Propst K, Swartzwelder HS, Kuhn CM (2008) Early ethanol consumption predicts relapse-like behavior in adolescent male rats. Alcohol Clin Exp Res 32:754–62
Schramm-Sapyta NL, Morris RW, Kuhn CM (2006) Adolescent rats are protected from the conditioned aversive properties of cocaine and lithium chloride. Pharmacol Biochem Behav 84:344–52
Schuckit M, Smith T, Pierson J, Danko G, Beltran IA (2006) Relationships among the level of response to alcohol and the number of alcoholic relatives in predicting alcohol-related outcomes. Alcohol Clin Exp Res 30:1308–14
Schuckit MA, Smith TL, Danko GP, Trim R, Bucholz KK, Edenberg HJ, Hesselbrock V, Kramer JJ, Dick DM (2009) An evaluation of the full level of response to alcohol model of heavy drinking and problems in COGA offspring. J Stud Alcohol Drugs 70:436–45
Schuckit MA, Tipp JE, Smith TL, Wiesbeck GA, Kalmijn J (1997) The relationship between Self-Rating of the Effects of alcohol and alcohol challenge results in ninety-eight young men. J Stud Alcohol 58:397–404
Schulte MT, Ramo D, Brown SA (2009) Gender differences in factors influencing alcohol use and drinking progression among adolescents. Clin Psychol Rev 29:535–47
Sherrill LK, Berthold C, Koss WA, Juraska JM, Gulley JM (2011) Sex differences in the effects of ethanol pre-exposure during adolescence on ethanol-induced conditioned taste aversion in adult rats. Behav Brain Res 225:104–9
Shram MJ, Funk D, Li Z, Le AD (2006) Periadolescent and adult rats respond differently in tests measuring the rewarding and aversive effects of nicotine. Psychopharmacology (Berl) 186:201–8
Siegmund S, Vengeliene V, Singer MV, Spanagel R (2005) Influence of age at drinking onset on long-term ethanol self-administration with deprivation and stress phases. Alcohol Clin Exp Res 29:1139–45
Simms JA, Steensland P, Medina B, Abernathy KE, Chandler LJ, Wise R, Bartlett SE (2008) Intermittent access to 20% ethanol induces high ethanol consumption in Long-Evans and Wistar rats. Alcohol Clin Exp Res 32:1816–23
Sinclair JD, Senter RJ (1968) Development of an alcohol-deprivation effect in rats. Q J Stud Alcohol 29:863–7
Spanagel R, Holter SM (1999) Long-term alcohol self-administration with repeated alcohol deprivation phases: an animal model of alcoholism? Alcohol Alcohol 34:231–43
van Haaren F, Anderson K (1994) Sex differences in schedule-induced alcohol consumption. Alcohol 11:35–40
Varlinskaya EI, Spear LP (2004a) Acute ethanol withdrawal (hangover) and social behavior in adolescent and adult male and female Sprague–Dawley rats. Alcohol Clin Exp Res 28:40–50
Varlinskaya EI, Spear LP (2004b) Changes in sensitivity to ethanol-induced social facilitation and social inhibition from early to late adolescence. Ann N Y Acad Sci 1021:459–61
Verendeev A, Riley AL (2012) Conditioned taste aversion and drugs of abuse: history and interpretation. Neurosci Biobehav Rev 36:2193–205
Vetter-O'Hagen C, Varlinskaya E, Spear L (2009) Sex differences in ethanol intake and sensitivity to aversive effects during adolescence and adulthood. Alcohol Alcohol 44:547–54
Vetter-O'Hagen CS, Spear LP (2011) The effects of gonadectomy on age- and sex-typical patterns of ethanol consumption in Sprague–Dawley rats. Alcohol Clin Exp Res 35:2039–49
Walker QD, Cabassa J, Kaplan KA, Li ST, Haroon J, Spohr HA, Kuhn CM (2001) Sex differences in cocaine-stimulated motor behavior: disparate effects of gonadectomy. Neuropsychopharmacology 25:118–30
Walker QD, Nelson CJ, Smith D, Kuhn CM (2002) Vaginal lavage attenuates cocaine-stimulated activity and establishes place preference in rats. Pharmacol Biochem Behav 73:743–52
Wilmouth CE, Spear LP (2004) Adolescent and adult rats' aversion to flavors previously paired with nicotine. Ann N Y Acad Sci 1021:462–4
York JL, Welte J, Hirsch J (2003) Gender comparison of alcohol exposure on drinking occasions. J Stud Alcohol 64:790–801
York JL, Welte JW (1994) Gender comparisons of alcohol consumption in alcoholic and nonalcoholic populations. J Stud Alcohol 55:743–50
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Schramm-Sapyta, N.L., Francis, R., MacDonald, A. et al. Effect of sex on ethanol consumption and conditioned taste aversion in adolescent and adult rats. Psychopharmacology 231, 1831–1839 (2014). https://doi.org/10.1007/s00213-013-3319-y
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DOI: https://doi.org/10.1007/s00213-013-3319-y