Sex differences in the effects of ethanol pre-exposure during adolescence on ethanol-induced conditioned taste aversion in adult rats

Behavioural Brain Research

Volumn 225, Issue 1, 2011, Pages 104-109

  Sherrill, Luke K ^a   Berthold, Claire ^a   Koss, Wendy A ^a   Juraska, Janice M ^a   Gulley, Joshua M ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Adolescence; Conditioned taste aversion; Ethanol; Sex differences; US pre exposure effect

Indexed keywords

ALCOHOL; SACCHARIN; SODIUM CHLORIDE;

ADOLESCENCE; ADULTHOOD; ALCOHOL CONSUMPTION; ANIMAL EXPERIMENT; ARTICLE; CONDITIONING; CONTROLLED STUDY; DRINKING BEHAVIOR; FEMALE; MALE; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; RAT; REWARD; SEX DIFFERENCE; TASTE AVERSION;

AGE FACTORS; ANALYSIS OF VARIANCE; ANIMALS; BLINKING; CENTRAL NERVOUS SYSTEM DEPRESSANTS; CONDITIONING, CLASSICAL; ETHANOL; FEMALE; FOOD PREFERENCES; HUMANS; MALE; RATS; RATS, LONG-EVANS; SACCHARIN; SEX CHARACTERISTICS; SWEETENING AGENTS; TASTE;

EID: 79960664963     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2011.07.003     Document Type: Article

References (73)

1. Samson H.H. Initiation of ethanol reinforcement using a sucrose-substitution procedure in food- and water-sated rats. Alcohol Clin Exp Res 1986, 10:436-442.
2. 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.
3. Hasin D.S., Stinson F.S., Ogburn E., Grant B.F. Prevalence, correlates, disability, and comorbidity of DSM-IV alcohol abuse and dependence in the United States: results from the National Epidemiologic Survey on Alcohol and Related Conditions. Arch Gen Psychiatry 2007, 64:830-842. 10.1001/archpsyc.64.7.830.
4. Patton G.C., McMorris B.J., Toumbourou J.W., Hemphill S.A., Donath S., Catalano R.F. Puberty and the onset of substance use and abuse. Pediatrics 2004, 114:e300-e306. 10.1542/peds.2003-0626-F.
5. Tschann J.M., Adler N.E., Irwin C.E., Millstein S.G., Turner R.A., Kegeles S.M. Initiation of substance use in early adolescence: the roles of pubertal timing and emotional distress. Health Psychol 1994, 13:326-333.
6. Wilson D.M., Killen J.D., Hayward C., Robinson T.N., Hammer L.D., Kraemer H.C., et al. Timing and rate of sexual maturation and the onset of cigarette and alcohol use among teenage girls. Arch Pediatr Adolesc Med 1994, 148:789-795.
7. Dick D.M., Rose R.J., Viken R.J., Kaprio J. Pubertal timing and substance use: associations between and within families across late adolescence. Dev Psychol 2000, 36:180-189.
8. Spear L.P. The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 2000, 24:417-463.
9. Smith R.F. Animal models of periadolescent substance abuse. Neurotoxicol Teratol 2003, 25:291-301.
10. Lancaster F.E., Brown T.D., Coker K.L., Elliott J.A., Wren S.B. Sex differences in alcohol preference and drinking patterns emerge during the early postpubertal period. Alcohol Clin Exp Res 1996, 20:1043-1049.
11. Truxell E.M., Molina J.C., Spear N.E. Ethanol intake in the juvenile, adolescent, and adult rat: effects of age and prior exposure to ethanol. Alcohol Clin Exp Res 2007, 31:755-765. 10.1111/j.1530-0277.2007.00358.x.
12. 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.
13. Brasser S.M., Spear N.E. Physiological and behavioral effects of acute ethanol hangover in juvenile, adolescent, and adult rats. Behav Neurosci 2002, 116:305-320.
14. Devaud L.L., Chadda R. Sex differences in rats in the development of and recovery from ethanol dependence assessed by changes in seizure susceptibility. Alcohol Clin Exp Res 2001, 25:1689-1696.
15. Wiren K.M., Hashimoto J.G., Alele P.E., Devaud L.L., Price K.L., Middaugh L.D., et al. Impact of sex: determination of alcohol neuroadaptation and reinforcement. Alcohol Clin Exp Res 2006, 30:233-242. 10.1111/j.1530-0277.2006.00032.x.
16. Veatch L.M., Wright T.M., Randall C.L. Only male mice show sensitization of handling-induced convulsions across repeated ethanol withdrawal cycles. Alcohol Clin Exp Res 2007, 31:477-485. 10.1111/j.1530-0277.2006.00328.x.
17. Sherrill L.K., Koss W.A., Foreman E.S., Gulley J.M. The effects of pre-pubertal gonadectomy and binge-like ethanol exposure during adolescence on ethanol drinking in adult male and female rats. Behav Brain Res 2011, 216:569-575. 10.1016/j.bbr.2010.08.048.
18. Witt E.D. Puberty, hormones, and sex differences in alcohol abuse and dependence. Neurotoxicol Teratol 2007, 29:81-95. 10.1016/j.ntt.2006.10.013.
19. Brockwell N.T., Eikelboom R., Beninger R.J. Caffeine-induced place and taste conditioning: production of dose-dependent preference and aversion. Pharmacol Biochem Behav 1991, 38:513-517.
20. Simpson G.R., Riley A.L. Morphine preexposure facilitates morphine place preference and attenuates morphine taste aversion. Pharmacol Biochem Behav 2005, 80:471-479. 10.1016/j.pbb.2005.01.003.
21. Wang Y.C., Huang A.C., Hsiao S. Paradoxical simultaneous occurrence of amphetamine-induced conditioned taste aversion and conditioned place preference with the same single drug injection: a new " pre- and post-association" experimental paradigm. Pharmacol Biochem Behav 2010, 95:80-87. 10.1016/j.pbb.2009.12.009.
22. Wise R.A., Yokel R.A., DeWit H. Both positive reinforcement and conditioned aversion from amphetamine and from apomorphine in rats. Science 1976, 191:1273-1275.
23. Strong M.N., Yoneyama N., Fretwell A.M., Snelling C., Tanchuck M.A., Finn D.A. Binge" drinking experience in adolescent mice shows sex differences and elevated ethanol intake in adulthood. Horm Behav 2009, 10.1016/j.yhbeh.2009.10.008.
24. 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. 10.1016/j.pbb.2010.07.008.
25. 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. 10.1111/j.1471-4159.2008.05835.x.
26. Chung C.S., Wang J., Wehman M., Rhoads D.E. Severity of alcohol withdrawal symptoms depends on developmental stage of Long-Evans rats. Pharmacol Biochem Behav 2008, 89:137-144. 10.1016/j.pbb.2007.12.002.
27. 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. 10.1111/j.1530-0277.2007.00534.x.
28. Riley A.L. The paradox of drug taking: the role of the aversive effects of drugs. Physiol Behav 2011, 103:69-78. 10.1016/j.physbeh.2010.11.021.
29. Conditioned Taste Aversion: An Annotated Bibliography. http://www.ctalearning.com/.
30. Riley A.L., Freeman K.B. Conditioned flavor aversions: assessment of drug-induced suppression of food intake. Curr Protoc Neurosci 2004, [Chapter 8:Unit 8.6E]. 10.1002/0471142301.ns0806es29.
31. Riley A.L., Simpson G.R. The attenuating effects of drug preexposure on taste aversion conditioning: generality, experimental parameters, underlying mechanisms and implications for drug use and abuse 2001, Lawrence Erlbaum Associates Publishers, Mahwah, NJ, US, 505 pp.
32. Riley A.L., Simpson G.R. Cocaine preexposure fails to sensitize the acquisition of cocaine-induced taste aversions. Pharmacol Biochem Behav 1999, 63:193-199.
33. Rabin B.M., Hunt W.A., Lee J. Attenuation and cross-attenuation in taste aversion learning in the rat: studies with ionizing radiation, lithium chloride and ethanol. Pharmacol Biochem Behav 1988, 31:909-918.
34. Holman E.W The effect of drug habituation before and after taste aversion learning in rats. Anim Learn Behav 1976, 4:329-332.
35. Berman R.F., Cannon D.S. The effect of prior ethanol experience on ethanol-induced saccharin aversions. Physiol Behav 1974, 12:1041-1044.
36. Cappell H., Le Blanc A.E. Conditioned aversion by amphetamine: rates of acquisition and loss of the attenuating effects of prior exposure. Psychopharmacologia 1975, 43:157-162.
37. Cappell H., LeBlanc A.E. Parametric investigations of the effects of prior exposure to amphetamine and morphine on conditioned gustatory aversion. Psychopharmacology (Berl) 1977, 51:265-271.
38. Barker L.M., Johns T. Effect of ethanol preexposure on ethanol-induced conditioned taste aversion. J Stud Alcohol 1978, 39:39-46.
39. Graham D.L., Diaz-Granados J.L. Periadolescent exposure to ethanol and diazepam alters the aversive properties of ethanol in adult mice. Pharmacol Biochem Behav 2006, 84:406-414. 10.1016/j.pbb.2006.05.024.
40. Hutchison M.A., Albaugh D.L., Riley A.L. Exposure to alcohol during adolescence alters the aversive and locomotor-activating effects of cocaine in adult rats. Pharmacol Biochem Behav 2010, 97:370-376. 10.1016/j.pbb.2010.09.006.
41. Hutchison M.A., Riley A.L. Adolescent exposure to nicotine alters the aversive effects of cocaine in adult rats. Neurotoxicol Teratol 2008, 30:404-411. 10.1016/j.ntt.2008.04.004.
42. Rinker J.A., Hutchison M.A., Chen S.A., Thorsell A., Heilig M., Riley A.L. Exposure to nicotine during periadolescence or early adulthood alters aversive and physiological effects induced by ethanol. Pharmacol Biochem Behav 2011, 99:7-16. 10.1016/j.pbb.2011.03.009.
43. Pascual M., Blanco A.M., Cauli O., Minarro 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. 10.1111/j.1460-9568.2006.05298.x.
44. Rinker J.A, Busse G.D., Roma P.G., Chen S.A., Barr C.S., Riley A.L. The effects of nicotine on ethanol-induced conditioned taste aversions in Long-Evans rats. Psychopharmacology (Berl) 2008, 197:409-419. 10.1007/s00213-007-1050-2.
45. Crabbe J.C., Feller D.J., Dorow J.S. Sensitivity and tolerance to ethanol-induced hypothermia in genetically selected mice. J Pharmacol Exp Ther 1989, 249:456-461.
46. Varlinskaya E.I., Spear L.P. Acute ethanol withdrawal (hangover) and social behavior in adolescent and adult male and female Sprague-Dawley rats. Alcohol Clin Exp Res 2004, 28:40-50. 10.1097/01.ALC.0000108655.51087.DF.
47. Orr T.E., Whitford-Stoddard J.L., Elkins R.L. Taste-aversion-prone (TAP) rats and taste-aversion-resistant (TAR) rats differ in ethanol self-administration, but not in ethanol clearance or general consumption. Alcohol 2004, 33:1-7. 10.1016/j.alcohol.2004.03.002.
48. Roma P.G, Flint W.W., Higley J.D., Riley A.L. Assessment of the aversive and rewarding effects of alcohol in Fischer and Lewis rats. Psychopharmacology (Berl) 2006, 189:187-199. 10.1007/s00213-006-0553-6.
49. Broadbent J., Muccino K.J., Cunningham C.L. Ethanol-induced conditioned taste aversion in 15 inbred mouse strains. Behav Neurosci 2002, 116:138-148.
50. Cannon D.S., Leeka J.K., Block A.K. Ethanol self-administration patterns and taste aversion learning across inbred rat strains. Pharmacol Biochem Behav 1994, 47:795-802.
51. Cailhol S., Mormede P. Conditioned taste aversion and alcohol drinking: strain and gender differences. J Stud Alcohol 2002, 63:91-99.
52. Chambers K.C., Yuan D., Brownson E.A., Wang Y. Sexual dimorphisms in conditioned taste aversions: mechanism and function. Learning, motivation, and cognition: the functional behaviorism of Robert C. Bolles 1997, 195-224. American Psychological Association, Washington, DC, US. M.E. Bouton, M.S. Fanselow (Eds.).
53. Chambers K.C., Sengstake C.B., Yoder R.L., Thornton J.E. Sexually dimorphic acquisition of a conditioned taste aversion in rats: effects of gonadectomy, testosterone replacement and water deprivation. Physiol Behav 1981, 27:83-88.
54. Randall-Thompson J.F, Riley A.L. Morphine-induced conditioned taste aversions: assessment of sexual dimorphism. Pharmacol Biochem Behav 2003, 76:373-381.
55. Busse G.D., Freeman K.B., Riley A.L. The interaction of sex and route of drug administration in cocaine-induced conditioned taste aversions. Pharmacol Biochem Behav 2005, 81:814-820. 10.1016/j.pbb.2005.06.004.
56. Vetter-O'Hagen C., Varlinskaya E., Spear L. Sex differences in ethanol intake and sensitivity to aversive effects during adolescence and adulthood. Alcohol Alcohol 2009, 44:547-554. 10.1093/alcalc/agp048.
57. Roma P.G., Davis C.M., Kohut S.J., Huntsberry M.E., Riley A.L. Early maternal separation and sex differences in the aversive effects of amphetamine in adult rats. Physiol Behav 2008, 93:897-904. 10.1016/j.physbeh.2007.12.007.
58. Jones J.D., Busse G.D., Riley A.L. Strain-dependent sex differences in the effects of alcohol on cocaine-induced taste aversions. Pharmacol Biochem Behav 2006, 83:554-560. 10.1016/j.pbb.2006.03.017.
59. Stock H.S., Caldarone B., Abrahamsen G., Mongeluzi D., Wilson M.A., Rosellini R.A. Sex differences in relation to conditioned fear-induced enhancement of morphine analgesia. Physiol Behav 2001, 72:439-447.
60. Beatty W.W., Beatty P.A. Hormonal determinants of sex differences in avoidance behavior and reactivity to electric shock in the rat. J Comp Physiol Psychol 1970, 73:446-455.
61. Pryce C.R., Lehmann J., Feldon J. Effect of sex on fear conditioning is similar for context and discrete CS in Wistar, Lewis and Fischer rat strains. Pharmacol Biochem Behav 1999, 64:753-759.
62. Itzhak Y., Roger-Sanchez C., Anderson K.L. Role of the nNOS gene in ethanol-induced conditioned place preference in mice. Alcohol 2009, 43:285-291. 10.1016/j.alcohol.2009.02.004.
63. Crippens D., White M.L., George M.A., Jaworski J.N., Brunner L.J., Lancaster F.E., et al. Gender differences in blood levels, but not brain levels, of ethanol in rats. Alcohol Clin Exp Res 1999, 23:414-420.
64. Goudie A.J, Dickins D.W. Nitrous oxide-induced conditioned taste aversions in rats: the role of duration of drug exposure and its relation to the taste aversion-self-administration " paradox" Pharmacol Biochem Behav 1978, 9:587-592.
65. Eckardt M.J. The role of orosensory stimuli from ethanol and blood-alcohol levels in producing conditioned taste aversion in the rat. Psychopharmacologia 1975, 44:267-271.
66. Roma P.G., Chen S.A., Barr C.S., Riley A.L. Dissociation between the aversive and pharmacokinetic effects of ethanol in female Fischer and Lewis rats. Behav Brain Res 2007, 182:51-56. 10.1016/j.bbr.2007.05.012.
67. Cunningham C.L, Clemans J.M., Fidler T.L. Injection timing determines whether intragastric ethanol produces conditioned place preference or aversion in mice. Pharmacol Biochem Behav 2002, 72:659-668.
68. Cannon D.S., Baker T.B., Berman R.F. Taste aversion disruption by drug pretreatment: dissociative and drug-specific effects. Pharmacol Biochem Behav 1977, 6:93-100.
69. Przybycien-Szymanska M.M., Mott N.N., Paul C.R., Gillespie R.A., Pak T.R. Binge-pattern alcohol exposure during puberty induces long-term changes in HPA axis reactivity. PLoS ONE 2011, 6:e18350. 10.1371/journal.pone.0018350.
70. 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. 10.1111/j.1530-0277.2007.00370.x.
71. Schulte M.T., Ramo D., Brown S.A. Gender differences in factors influencing alcohol use and drinking progression among adolescents. Clin Psychol Rev 2009, 29:535-547. 10.1016/j.cpr.2009.06.003.
72. Vetter-O'Hagen C.S., Spear L.P. The effects of gonadectomy on age- and sex-typical patterns of ethanol consumption in Sprague-Dawley rats. Alcohol Clin Exp Res 2011, 10.1111/j.1530-0277.2011.01555.x.
73. 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.