The effects of pre-pubertal gonadectomy and binge-like ethanol exposure during adolescence on ethanol drinking in adult male and female rats

Behavioural Brain Research

Volumn 216, Issue 2, 2011, Pages 569-575

  Sherrill, Luke K ^a   Koss, Wendy A ^a   Foreman, Emily S ^a   Gulley, Joshua M ^a  

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

Author keywords

Adolescence; Ethanol self administration; Gonadectomy; Ovariectomy; Sex differences

Indexed keywords

ALCOHOL; SEX HORMONE; SUCROSE;

ADOLESCENCE; ADULT ANIMAL; ALCOHOL CONSUMPTION; ALCOHOL INTOXICATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DRINKING BEHAVIOR; FEMALE; GONADECTOMY; LONG EVANS RAT; MALE; NONHUMAN; OVARIECTOMY; PERINATAL PERIOD; PREPUBERTY; PRIORITY JOURNAL; RAT; SEX DIFFERENCE;

AGE FACTORS; ANALYSIS OF VARIANCE; ANIMALS; CENTRAL NERVOUS SYSTEM DEPRESSANTS; CRITICAL PERIOD (PSYCHOLOGY); DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRINKING BEHAVIOR; ETHANOL; FEMALE; FOOD PREFERENCES; GONADAL STEROID HORMONES; MALE; PUBERTY; RATS; RATS, LONG-EVANS; SEX FACTORS; SUCROSE; SWEETENING AGENTS;

EID: 78149497117     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2010.08.048     Document Type: Article

References (92)

1. Almeida O.F., Shoaib M., Deicke J., Fischer D., Darwish M.H., Patchev V.K. Gender differences in ethanol preference and ingestion in rats. The role of the gonadal steroid environment. J Clin Invest 1998, 101:2677-2685. 10.1172/JCI1198.
2. Andersen S.L., Thompson A.T., Rutstein M., Hostetter J.C., Teicher M.H. Dopamine receptor pruning in prefrontal cortex during the periadolescent period in rats. Synapse 2000, 37:167-169. doi: 2-B.
3. 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.
4. Becker H.C, Anton R.F., De Trana C., Randall C.L. Sensitivity to ethanol in female mice: effects of ovariectomy and strain. Life Sci 1985, 37:1293-1300.
5. 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.
6. 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.
7. Bujas M., Pericic D., Jazvinscak M. Influence of gender and gonadectomy on bicuculline-induced convulsions and on GABAA receptors. Brain Res Bull 1997, 43:411-416.
8. Cailhol S., Mormede P. Sex and strain differences in ethanol drinking: effects of gonadectomy. Alcohol Clin Exp Res 2001, 25:594-599.
9. Cameron J.L. Interrelationships between hormones, behavior, and affect during adolescence: understanding hormonal, physical, and brain changes occurring in association with pubertal activation of the reproductive axis. Introduction to part III. Ann N Y Acad Sci 2004, 1021:110-123. 10.1196/annals.1308.012.
10. 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.
11. Clarke S.N, Ossenkopp K.P. Taste reactivity responses in rats: influence of sex and the estrous cycle. Am J Physiol 1998, 274:R718-R724.
12. Cunningham M.G., Bhattacharyya S., Benes F.M. Amygdalo-cortical sprouting continues into early adulthood: implications for the development of normal and abnormal function during adolescence. J Comp Neurol 2002, 453:116-130. 10.1002/cne.10376.
13. Czachowski C.L., Samson H.H., Denning C.E. Blood ethanol concentrations in rats drinking sucrose/ethanol solutions. Alcohol Clin Exp Res 1999, 23:1331-1335.
14. Dar M.S. Antagonism by intracerebellar Ro15-4513 of acute ethanol-induced motor incoordination in mice. Pharmacol Biochem Behav 1995, 52:217-223.
15. 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.
16. 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.
17. Dinopoulos A., Dori I., Parnavelas J.G. The serotonin innervation of the basal forebrain shows a transient phase during development. Brain Res Dev Brain Res 1997, 99:38-52.
18. Dohler K.D., Wuttke W. Changes with age in levels of serum gonadotropins, prolactin and gonadal steroids in prepubertal male and female rats. Endocrinology 1975, 97:898-907.
19. 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.
20. 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 Res 2008, 1215:40-52. 10.1016/j.brainres.2008.03.056.
21. Eade A.M, Youngentob S.L. Adolescent ethanol experience alters immediate and long-term behavioral responses to ethanol odor in observer and demonstrator rats. Behav Brain Funct 2009, 5:23. 10.1186/1744-9081-5-23.
22. Ford M.M., Eldridge J.C., Samson H.H. Ethanol consumption in the female Long-Evans rat: a modulatory role of estradiol. Alcohol 2002, 26:103-113.
23. Gauvin D.V., Moore K.R., Holloway F.A. Do rat strain differences in ethanol consumption reflect differences in ethanol sensitivity or the preparedness to learn?. Alcohol 1993, 10:37-43.
24. Giedd J.N., Vaituzis A.C., Hamburger S.D., Lange N., Rajapakse J.C., Kaysen D., et al. Quantitative MRI of the temporal lobe, amygdala, and hippocampus in normal human development: ages 4-18 years. J Comp Neurol 1996, 366:223-230. doi: 2-7.
25. Giedd J.N., Blumenthal J., Jeffries N.O., Castellanos F.X., Liu H., Zijdenbos A., et al. Brain development during childhood and adolescence: a longitudinal MRI study. Nat Neurosci 1999, 2:861-863. 10.1038/13158.
26. Gililland K.R., Finn D.A. The impact of gonadectomy and adrenalectomy on acute withdrawal severity in male and female C57BL/6J and DBA/2J mice following a single high dose of ethanol. Alcohol Clin Exp Res 2007, 31:1846-1857. 10.1111/j.1530-0277.2007.00509.x.
27. 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.
28. Greenfield T.K., Rogers J.D. Who drinks most of the alcohol in the US? The policy implications. J Stud Alcohol 1999, 60:78-89.
29. 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.
30. Juarez J., Vazquez-Cortes C., Barrios-De Tomasi E. Different stages in the temporal course of estrogen treatment produce opposite effects on voluntary alcohol consumption in male rats. Alcohol 2005, 36:55-61. 10.1016/j.alcohol.2005.06.003.
31. Jung M.E, Yang S.H., Brun-Zinkernagel A.M., Simpkins J.W. Estradiol protects against cerebellar damage and motor deficit in ethanol-withdrawn rats. Alcohol 2002, 26:83-93.
32. Juraska J.M., Markham J.A. The cellular basis for volume changes in the rat cortex during puberty: white and gray matter. Ann N Y Acad Sci 2004, 1021:431-435. 10.1196/annals.1308.058.
33. Kaffman A., Meaney M.J. Neurodevelopmental sequelae of postnatal maternal care in rodents: clinical and research implications of molecular insights. J Child Psychol Psychiatry 2007, 48:224-244. 10.1111/j.1469-7610.2007.01730.x.
34. Kaufman K.R, Tanchuck M.A., Strong M.N., Finn D.A. Replacement with GABAergic steroid precursors restores the acute ethanol withdrawal profile in adrenalectomy/gonadectomy mice. Neuroscience 2010, 166:5-14. 10.1016/j.neuroscience.2009.11.075.
35. Knoll J, Miklya I., Knoll B., Dallo J. Sexual hormones terminate in the rat: the significantly enhanced catecholaminergic/serotoninergic tone in the brain characteristic to the post-weaning period. Life Sci 2000, 67:765-773.
36. Lakoza G.N., Barkov N.K. The role of testosterone in the development of experimental alcoholism. Bull Narc 1980, 32:41-48.
37. 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.
38. Lauing K., Himes R., Rachwalski M., Strotman P., Callaci J.J. Binge alcohol treatment of adolescent rats followed by alcohol abstinence is associated with site-specific differences in bone loss and incomplete recovery of bone mass and strength. Alcohol 2008, 42:649-656. 10.1016/j.alcohol.2008.08.005.
39. Le A.D, Israel Y., Juzytsch W., Quan B., Harding S. Genetic selection for high and low alcohol consumption in a limited-access paradigm. Alcohol Clin Exp Res 2001, 25:1613-1620.
40. Lenroot R.K., Giedd J.N. Sex differences in the adolescent brain. Brain Cogn 2010, 72:46-55. 10.1016/j.bandc.2009.10.008.
41. Levin E.D, Lawrence S.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. Neurotoxicol Teratol 2007, 29:458-465. 10.1016/j.ntt.2007.02.002.
42. Litteria M Long-term effects of neonatal ovariectomy on cerebellar development in the rat: a histological and morphometric study. Brain Res Dev Brain Res 1994, 81:113-120.
43. Majchrowicz E. Induction of physical dependence upon ethanol and the associated behavioral changes in rats. Psychopharmacologia 1975, 43:245-254.
44. Maldonado A.M., Finkbeiner L.M., Alipour K.K., Kirstein C.L. Voluntary ethanol consumption differs in adolescent and adult male rats using a modified sucrose-fading paradigm. Alcohol Clin Exp Res 2008, 32:1574-1582. 10.1111/j.1530-0277.2008.00733.x.
45. Markham J.A, Morris J.R., Juraska J.M. Neuron number decreases in the rat ventral, but not dorsal, medial prefrontal cortex between adolescence and adulthood. Neuroscience 2007, 144:961-968. 10.1016/j.neuroscience.2006.10.015.
46. 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. 10.1016/j.alcohol.2008.09.001.
47. Meaney M.J, Aitken D.H. The effects of early postnatal handling on hippocampal glucocorticoid receptor concentrations: temporal parameters. Brain Res 1985, 354:301-304.
48. Mezey E. Influence of sex hormones on alcohol metabolism. Alcohol Clin Exp Res 2000, 24:421.
49. Mitsushima D., Hei D.L., Terasawa E. Gamma-Aminobutyric acid is an inhibitory neurotransmitter restricting the release of luteinizing hormone-releasing hormone before the onset of puberty. Proc Natl Acad Sci U S A 1994, 91:395-399.
50. Moore C.L, Chadwick-Dias A.M. Behavioral responses of infant rats to maternal licking: variations with age and sex. Dev Psychobiol 1986, 19:427-438. 10.1002/dev.420190504.
51. Moore E.M., Mariani J.N., Linsenbardt D.N., Melon 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, 10.1111/j.1530-0277.2009.01143.x.
52. Muller R.A., Rothermel R.D., Behen M.E., Muzik O., Mangner T.J., Chugani H.T. Developmental changes of cortical and cerebellar motor control: a clinical positron emission tomography study with children and adults. J Child Neurol 1998, 13:550-556.
53. 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.
54. 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.
55. Philpot R., Kirstein C. Developmental differences in the accumbal dopaminergic response to repeated ethanol exposure. Ann N Y Acad Sci 2004, 1021:422-426. 10.1196/annals.1308.056.
56. Philpot R.M., Wecker L., Kirstein C.L. Repeated ethanol exposure during adolescence alters the developmental trajectory of dopaminergic output from the nucleus accumbens septi. Int J Dev Neurosci 2009, 27:805-815. 10.1016/j.ijdevneu.2009.08.009.
57. Piazza N.J, Vrbka J.L., Yeager R.D. Telescoping of alcoholism in women alcoholics. Int J Addict 1989, 24:19-28.
58. Przybycien-Szymanska M.M., Rao Y.S., Pak T.R. Binge-pattern alcohol exposure during puberty induces sexually dimorphic changes in genes regulating the HPA axis. Am J Physiol Endocrinol Metab 2009, 10.1152/ajpendo.00615.2009.
59. Quintanilla M.E., Tampier L., Sapag A., Gerdtzen Z., Israel Y. Sex differences, alcohol dehydrogenase, acetaldehyde burst, and aversion to ethanol in the rat: a systems perspective. Am J Physiol Endocrinol Metab 2007, 293:E531-E537. 10.1152/ajpendo.00187.2007.
60. Rewal M., Jung M.E., Simpkins J.W. Role of the GABA-A system in estrogen-induced protection against brain lipid peroxidation in ethanol-withdrawn rats. Alcohol Clin Exp Res 2004, 28:1907-1915.
61. Rewal M., Jung M.E., Wen Y., Brun-Zinkernagel A.M., Simpkins J.W. Role of the GABAA system in behavioral, motoric, and cerebellar protection by estrogen during ethanol withdrawal. Alcohol 2003, 31:49-61.
62. Robinson D.L., Brunner L.J., Gonzales R.A. Effect of gender and estrous cycle on the pharmacokinetics of ethanol in the rat brain. Alcohol Clin Exp Res 2002, 26:165-172.
63. Rodd-Henricks Z.A., Bell R.L., Kuc K.A., Murphy J.M., McBride W.J., Lumeng L., et al. Effects of ethanol exposure on subsequent acquisition and extinction of ethanol self-administration and expression of alcohol-seeking behavior in adult alcohol-preferring (P) rats: I periadolescent exposure. Alcohol Clin Exp Res 2002, 26:1632-1641. 10.1097/01.ALC.0000036301.36192.BC.
64. Rubinow M.J., Juraska J.M. Neuron and glia numbers in the basolateral nucleus of the amygdala from preweaning through old age in male and female rats: a stereological study. J Comp Neurol 2009, 512:717-725. 10.1002/cne.21924.
65. Russo S.J., Festa E.D., Fabian S.J., Gazi F.M., Kraish M., Jenab S., et al. Gonadal hormones differentially modulate cocaine-induced conditioned place preference in male and female rats. Neuroscience 2003, 120:523-533.
66. SAMHSA Results from the 2008 national survey on drug use and health: national findings 2009, Office of Applied Studies, NSDUH Series H-36, HHS Publication No. SMA 09-4434, Rockville, MD.
67. 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.
68. Siegmund S., Vengeliene V., Singer M.V., Spanagel R. Influence of age at drinking onset on long-term ethanol self-administration with deprivation and stress phases. Alcohol Clin Exp Res 2005, 29:1139-1145.
69. Silveri M.M., Spear L.P. Acute, rapid, and chronic tolerance during ontogeny: observations when equating ethanol perturbation across age. Alcohol Clin Exp Res 2001, 25:1301-1308.
70. 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. 10.1097/01.ALC.0000090141.66526.22.
71. Slawecki C.J. Two-choice reaction time performance in Sprague-Dawley rats exposed to alcohol during adolescence or adulthood. Behav Pharmacol 2006, 17:605-614. 10.1097/01.fbp.0000236272.10418.62.
72. Slawecki C.J, Betancourt M. Effects of adolescent ethanol exposure on ethanol consumption in adult rats. Alcohol 2002, 26:23-30.
73. Slob A.K., Van der Werff Ten Bosch J.J. Sex differences in body growth in the rat. Physiol Behav 1975, 14:353-361.
74. 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. 10.1016/j.pbb.2007.02.008.
75. 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.
76. Stuart E.B., Thompson J.M., Rhees R.W., Lephart E.D. Steroid hormone influence on brain calbindin-D(28 K) in male prepubertal and ovariectomized rats. Brain Res Dev Brain Res 2001, 129:125-133.
77. Suzdak P.D., Schwartz R.D., Skolnick P., Paul S.M. Alcohols stimulate gamma-aminobutyric acid receptor-mediated chloride uptake in brain vesicles: correlation with intoxication potency. Brain Res 1988, 444:340-345.
78. Swartzwelder H.S., Richardson R.C., Markwiese-Foerch B., Wilson W.A., Little P.J. Developmental differences in the acquisition of tolerance to ethanol. Alcohol 1998, 15:311-314.
79. Tambour S., Brown L.L., Crabbe J.C. Gender and age at drinking onset affect voluntary alcohol consumption but neither the alcohol deprivation effect nor the response to stress in mice. Alcohol Clin Exp Res 2008, 32:2100-2106. 10.1111/j.1530-0277.2008.00798.x.
80. Tiemeier H, Lenroot R.K., Greenstein D.K., Tran L., Pierson R., Giedd J.N. Cerebellum development during childhood and adolescence: a longitudinal morphometric MRI study. Neuroimage 2010, 49:63-70. 10.1016/j.neuroimage.2009.08.016.
81. Torres O.V, Natividad L.A., Tejeda H.A., Van Weelden S.A., O'Dell L.E. Female rats display dose-dependent differences to the rewarding and aversive effects of nicotine in an age-, hormone-, and sex-dependent manner. Psychopharmacology (Berl) 2009, 206:303-312. 10.1007/s00213-009-1607-3.
82. 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.
83. 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.
84. Varlinskaya E.I., Spear L.P. Sensitization to social anxiolytic effects of ethanol in adolescent and adult Sprague-Dawley rats after repeated ethanol exposure. Alcohol 2010, 44:99-110. 10.1016/j.alcohol.2009.09.036.
85. 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. 10.1111/j.1530-0277.2007.00417.x.
86. 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.
87. Wezeman F.H., Juknelis D., Frost N., Callaci J.J. Spine bone mineral density and vertebral body height are altered by alcohol consumption in growing male and female rats. Alcohol 2003, 31:87-92.
88. 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.
89. 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.
90. Yu Z.Y, Wang W., Fritschy J.M., Witte O.W., Redecker C. Changes in neocortical and hippocampal GABAA receptor subunit distribution during brain maturation and aging. Brain Res 2006, 1099:73-81. 10.1016/j.brainres.2006.04.118.
91. Zhang L, Warren R.A. Postnatal development of excitatory postsynaptic currents in nucleus accumbens medium spiny neurons. Neuroscience 2008, 154:1440-1449. 10.1016/j.neuroscience.2008.05.002.
92. Zucker I Hormonal determinants of sex differences in saccharin preference, food intake and body weight. Physiology behavior 1969, 4:595-602.