Sex differences in the long-lasting consequences of adolescent ethanol exposure for the rewarding effects of cocaine in mice

Psychopharmacology

Volumn 232, Issue 16, 2015, Pages 2995-3007

  Mateos Garcia A ^a   Manzanedo, C ^a   Rodriguez Arias M ^a   Aguilar, M A ^a   Reig Sanchis, E ^a   Navarro Frances C I ^a   Valverde, O ^b   Minarro J ^a   Arenas, M C ^a  

^a UNIVERSITY OF VALENCIA   (Spain)

^b UNIVERSITAT POMPEU FABRA   (Spain)

Author keywords

Adolescence; Binge drinking; Cocaine; CPP; Ethanol; Intravenous self administration; Mice; Sex differences

Indexed keywords

ALCOHOL; COCAINE; DOPAMINE UPTAKE INHIBITOR;

ADOLESCENT; ADULT; ANIMAL EXPERIMENT; ARTICLE; BINGE DRINKING; CONCENTRATION RESPONSE; CONTROLLED STUDY; FEMALE; LOCOMOTION; MALE; MOUSE; NONHUMAN; PLACE PREFERENCE; PRIORITY JOURNAL; REWARD; SELF ADMINISTRATION TEST; SEX DIFFERENCE; AGE; ANIMAL; ANIMAL BEHAVIOR; CONDITIONING; DRUG EFFECTS; DRUG SELF ADMINISTRATION; HUMAN; MOTOR ACTIVITY; SEXUAL DEVELOPMENT;

ADOLESCENT; AGE FACTORS; ANIMALS; BEHAVIOR, ANIMAL; COCAINE; CONDITIONING (PSYCHOLOGY); DOPAMINE UPTAKE INHIBITORS; ETHANOL; FEMALE; HUMANS; MALE; MICE; MOTOR ACTIVITY; REWARD; SELF ADMINISTRATION; SEX CHARACTERISTICS;

EID: 84937972981     PISSN: 00333158     EISSN: 14322072     Source Type: Journal    
DOI: 10.1007/s00213-015-3937-7     Document Type: Article

References (64)

1. Aguilar MA, Rodríguez-Arias M, Miñarro J (2009) Neurobiological mechanisms of the reinstatement of drug-conditioned place preference. Brain Res Rev 59:253-77. doi: 10.1016/j.brainresrev.2008.08.002
2. Alaux-Cantin S, Warnault V, Legastelois R, Botia B, Pierrefiche O, Vilpoux C, Naassila M (2013) Alcohol intoxications during adolescence increase motivation for alcohol in adult rats and induce neuroadaptations in the nucleus accumbens. Neuropharmacology 67:521-31. doi: 10.1016/j.neuropharm.2012.12.007
3. Alfonso-Loeches S, Guerri C (2011) Molecular and behavioral aspects of the actions of alcohol on the adult and developing brain. Crit Rev Clin Lab Sci 48:19-47. doi: 10.3109/10408363.2011.580567
4. Anker JJ, Carroll ME (2011) Females are more vulnerable to drug abuse than males: evidence from preclinical studies and the role of ovarian hormones. Curr Top Behav Neurosci 8:73-96. doi: 10.1007/7854-2010-93
5. Arenas MC, Daza-Losada M, Vidal-Infer A, Aguilar MA, Miñarro J, Rodríguez-Arias M (2014) Capacity of novelty-induced locomotor activity and the hole-board test to predict sensitivity to the conditioned rewarding effects of cocaine. Physiol Behav 22(133):152-60. doi: 10.1016/j.physbeh.2014.05.028
6. Arias F, Szerman N, Vega P, Mesias B, Basurte I, Morant C, Ochoa E, Poyo F, Babin F (2013) Cocaine abuse or dependency and other pyschiatric disorders. Madrid study on dual pathology. Rev Psiquiatr Salud Ment 6:121-8. doi: 10.1016/j.rpsm.2012.09.002
7. Badanich KA, Maldonado AM, Kirstein CL (2007) Chronic ethanol exposure during adolescence increases basal dopamine in the nucleus accumbens septi during adulthood. Alcohol Clin Exp Res 31:895-900
8. Becker JB, Hu M (2008) Sex differences in drug abuse. Front Neuroendocrinol 29:36-47
9. Boutros N, Semenova S, Markou A (2014) Adolescent intermittent ethanol exposure diminishes anhedonia during ethanol withdrawal in adulthood. Eur Neuropsychopharmacol 24:856-64. doi: 10.1016/j.euroneuro.2014.01.022
10. Cable N, Sacker A (2008) Typologies of alcohol consumption in adolescence: predictors and adult outcomes. Alcohol Alcohol 43:81-90
11. Carroll ME, Morgan AD, Lynch WJ, Campbell UC, Dess NK (2002) Intravenous cocaine and heroin self-administration in rats selectively bred for differential saccharin intake: phenotype and sex differences. Psychopharmacology (Berl) 161:304-313
12. Centers for Disease Control (2013) Youth Risk Behavior Surveillance System (YRBSS). Available at: http://www.cdc.gov/healthyyouth/yrbs/index.htm
13. Crews F, He J, Hodge C (2007) Adolescent cortical development: a critical period of vulnerability for addiction. Pharmacol Biochem Behav 86(2):189-99
14. Dalla C, Shors TJ (2009) Sex differences in learning processes of classical and operant conditioning. Physiol Behav 97:229-38. doi: 10.1016/j.physbeh.2009.02.035
15. Degenhardt L, O'Loughlin C, Swift W, Romaniuk H, Carlin J, Coffey C, Hall W, Patton G (2013) The persistence of adolescent binge drinking into adulthood: findings from a 15-year prospective cohort study. BMJ Open 3, e003015. doi: 10.1136/bmjopen-2013-003015
16. Do Couto BR, Rodríguez-Arias M, Fuentes S, Gagliano H, Armario A, Miñarro J, Aguilar MA (2011) Adolescent pre-exposure to ethanol or MDMA prolongs the conditioned rewarding effects of MDMA. Physiol Behav 103:585-93. doi: 10.1016/j.physbeh.2011.02.012
17. 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
18. ESTUDES (2013) Informe de la encuesta estatal sobre el uso de drogas en estudiantes de enseñanzas secundarias. Delegación del gobierno para el Plan Nacional sobre Drogas website. Ministerio de Sanidad y Política Social, Gobierno de España, Available: http://www.pnsd.msc.es/Categoria2/observa/pdf/PresentESTUDES2012-2013.pdf
19. Grant BF, Stinson FS, Harford TC (2001) Age at onset of alcohol use and DSM-IV alcohol abuse and dependence: a 12-year follow-up. J Subst Abuse 13:493-504
20. Guerri C (2002) Mechanisms involved in central nervous system dysfunctions induced by prenatal ethanol exposure. Neurotox Res 4:327-35
21. Harper C, Matsumoto I (2005) Ethanol and brain damage. Curr Opin Pharmacol 5:73-8
22. Hibell B, Guttormsson U, Ahlström S, et al (2012) The 2011 ESPAD Report: Substance use among students in 36 European Countries. Stockholm: The Swedish Council for Information on Alcohol and other Drugs (CAN) The European Monitoring Centre for Drugs and Drug Addiction (EMCDDA), Council of Europe, Co-operation Group to Combat Drug Abuse and Illicit Trafficking in Drugs (Pompidou Group). Available: http://www.espad.org/Uploads/ESPAD-reports/2011/The-2011-ESPAD-Report-FULL-2012-10-29.pdf
23. Hingson RW, Heeren T, Winter MR (2006) Age at drinking onset and alcohol dependence: age at onset, duration, and severity. Arch Pediatr Adolesc Med 160:739-46
24. Hutchison MA, Albaugh DL, Riley AL (2010) Exposure to alcohol during adolescence alters the aversive and locomotor-activating effects of cocaine in adult rats. Pharmacol Biochem Behav 97:370-6. doi: 10.1016/j.pbb.2010.09.006
25. Hutchison MA, Riley AL (2012) Ethanol exposure during either adolescence or adulthood alters the rewarding effects of cocaine in adult rats. Pharmacol Biochem Behav 101:458-64. doi: 10.1016/j.pbb.2012.02.007
26. Johnston LD, O'Malley PM, Bachman JG, Schulenberg JE (2013) Monitoring the Future: National survey results on drug use, 1975-2012; 2012 Overview; Key Findings on Adolescent Drug Use. (Ann Arbor: Institute for Social Research, The University of Michigan). Available: http://www.monitoringthefuture.org/pubs/monographs/mtf-overview2013.pdf
27. Kandel DB, Yamaguchi K, Chen K (1992) Stages of progression in drug involvement from adolescence to adulthood: further evidence for the gateway theory. J Stud Alcohol 53:447-57
28. Koss WA, Sadowski RN, Sherrill LK, Gulley JM, Juraska JM (2012) Effects of ethanol during adolescence on the number of neurons and glia in the medial prefrontal cortex and basolateral amygdala of adult male and female rats. Brain Res 1466:24-32. doi: 10.1016/j.brainres.2012.05.023
29. Lynch WJ, Carroll ME (1999) Sex differences in the acquisition of intravenously self-administered cocaine and heroin in rats. Psychopharmacology (Berl) 144:77-82
30. Manzanedo C, Aguilar MA, Rodríguez-Arias M, Miñarro J (2001) Effects of dopamine antagonists with different receptor blockade profiles on morphine-induced place preference in male mice. Behav Brain Res 121:189-97
31. Martini M, Pinto AX, Valverde O (2014) Estrous cycle and sex affect cocaine-induced behavioural changes in CD1 mice. Psychopharmacology 231:2647-59. doi: 10.1007/s00213-014-3433-5
32. Martini M, Valverde O (2012) A single episode of maternal deprivation impairs the motivation for cocaine in adolescent mice. Psychopharmacology 219:149-158. doi: 10.1007/s00213-011-2385-2
33. Mateos-García A, Roger-Sánchez C, Rodriguez-Arias M, Miñarro J, Aguilar MA, Manzanedo C, Arenas MC (2015) Higher sensitivity to the conditioned rewarding effects of cocaine and MDMA in High-Novelty-Seekers mice exposed to a cocaine binge during adolescence. Psychopharmacology 232(1):101-13. doi: 10.1007/s00213-014-3642-y
34. McClain JA, Morris SA, Marshall SA, Nixon K (2014) Ectopic hippocampal neurogenesis in adolescent male rats following alcohol dependence. Addict Biol 19:687-99. doi: 10.1111/adb.12075
35. Molet J, Bouaziz E, Hamon M, Lanfumey L (2012) Early exposure to ethanol differentially affects ethanol preference at adult age in two inbred mouse strains. Neuropharmacology 63:338-48. doi: 10.1016/j.neuropharm.2012.03.028
36. Molet J, Hervé D, Thiébot MH, Hamon M, Lanfumey L (2013) Juvenile ethanol exposure increases rewarding properties of cocaine and morphine in adult DBA/2 J mice. Eur Neuropsychopharmacol 23:1816-25. doi: 10.1016/j.euroneuro.2013.03.010
37. Montagud-Romero S, Daza-Losada M, Vidal-Infer A, Maldonado C, Aguilar MA, Miñarro J, Rodríguez-Arias M (2014) The novelty-seeking phenotype modulates the long-lasting effects of intermittent ethanol administration during adolescence. PLoS One 9, e92576. doi: 10.1371/journal.pone.0092576
38. Navarro-Francés CI, Arenas MC (2014) Influence of trait anxiety on the effects of acute stress on learning and retention of the passive avoidance task in male and female mice. Behav Process 105:6-14. doi: 10.1016/j.beproc.2014.02.009
39. Newsletter NIAAA (2004) National Institute of Alcohol Abuse and Alcoholism. Department of health and human Services-National Institutes of Health website. Office of Research Translation and Communications, Bethesda, Maryland, Available: http://pubs.niaaa.nih.gov/publications/Newsletter/winter2004/Newsletter-Number3.pdf
40. Pascual M, Blanco AM, Cauli O, Miñarro J, Guerri C (2007) Intermittent ethanol exposure induces inflammatory brain damage and causes long-term behavioural alterations in adolescent rats. Eur J Neurosci 25:541-50
41. Pascual M, Boix J, Felipo V, Guerri C (2009) Repeated alcohol administration during adolescence causes changes in the mesolimbic dopaminergic and glutamatergic systems and promotes alcohol intake in the adult rat. J Neurochem 108:920-31. doi: 10.1111/j.1471-4159.2008.05835.x
42. Pascual M, Do Couto BR, Alfonso-Loeches S, Aguilar MA, Rodriguez-Arias M, Guerri C (2012) Changes in histone acetylation in the prefrontal cortex of ethanol-exposed adolescent rats are associated with ethanol-induced place conditioning. Neuropharmacology 62:2309-19. doi: 10.1016/j.neuropharm.2012.01.011
43. Philpot RM, Wecker L, Kirstein CL (2009) Repeated ethanol exposure during adolescence alters the developmental trajectory of dopaminergic output from the nucleus accumbens septi. Int J Dev Neurosci 27:805-15. doi: 10.1016/j.ijdevneu.2009.08.009
44. Quoilin C, Didone V, Tirelli E, Quertemont E (2014) Higher long-lasting ethanol sensitization after adolescent ethanol exposure in mice. Psychopharmacology 231:1821-9. doi: 10.1007/s00213-013-3376-2
45. Richardson NR, Roberts DC (1996) Progressive ratio schedules in drug self-administration studies in rats: a method to evaluate reinforcing efficacy. J Neurosci Methods 66:1-11
46. Riley AL (2011) The paradox of drug taking: the role of the aversive effects of drugs. Physiol Behav 103:69-78. doi: 10.1016/j.physbeh.2010.11.021
47. Rodríguez-Arias M, Maldonado C, Vidal-Infer A, Guerri C, Aguilar MA, Miñarro J (2011) Intermittent ethanol exposure increases long-lasting behavioural and neurochemical effects of MDMA in adolescent mice. Psychopharmacology 218:429-442. doi: 10.1007/s00213-011-2329-x
48. Roger-Sanchez C, Aguilar MA, Rodríguez-Arias M, Aragon CM, Miñarro J (2012) Age- and sex-related differences in the acquisition and reinstatement of ethanol CPP in mice. Neurotoxicol Teratol 34:108-15. doi: 10.1016/j.ntt.2011.07.011
49. Sherrill LK, Berthold C, Koss WA, Juraska JM, Gulley JM (2011a) 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. doi: 10.1016/j.bbr.2011.07.003
50. Sherrill LK, Koss WA, Foreman ES, Gulley JM (2011b) 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 216:569-75. doi: 10.1016/j.bbr.2010.08.048
51. Soria G, Mendizabal V, Tourino C, Robledo P, Ledent C, Parmentier M, Maldonado R, Valverde O (2005) Lack of CB1 cannabinoid receptor impairs cocaine self-administration. Neuropsychopharmacology 30:1670-1680
52. Spear LP, Swartzwelder HS (2014) Adolescent alcohol exposure and persistence of adolescent-typical phenotypes into adulthood: a mini-review. Neurosci Biobehav Rev 45C:1-8. doi: 10.1016/j.neubiorev.2014.04.012
53. Spear LP, Varlinskaya EI (2005) Adolescence. Alcohol sensitivity, tolerance, and intake. Recent Dev Alcohol 17:143-59
54. Tarazi FI, Baldessarini RJ (2000) Comparative postnatal development of dopamine D(1), D(2) and D(4) receptors in rat forebrain. Int J Dev Neurosci 18:29-37
55. Tzschentke TM (1998) Measuring reward with the conditioned place preference paradigm: a comprehensive review of drug effects, recent progress and new issues. Prog Neurobiol 56:613-72. doi: 10.1016/S0301-0082(98)00060-4
56. Tzschentke TM (2007) Measuring reward with the conditioned place preference (CPP) paradigm: update of the last decade. Addict Biol 12:227-462. doi: 10.1111/j.1369-1600.2007.00070.x
57. Varlinskaya EI, Spear LP (2002) Acute effects of ethanol on social behavior of adolescent and adult rats: role of familiarity of the test situation. Alcohol Clin Exp Res 26:1502-11
58. Varlinskaya EI, Truxell E, Spear LP (2014) Chronic intermittent ethanol exposure during adolescence: effects on social behavior and ethanol sensitivity in adulthood. Alcohol 48:433-44. doi: 10.1016/j.alcohol.2014.01.012
59. Verendeev A, Riley AL (2012) Conditioned taste aversion and drugs of abuse: history and interpretation. Neurosci Biobehav Rev 36(10):2193-205. doi: 10.1016/j.neubiorev.2012.08.004
60. Verendeev A, Riley AL (2013) The role of the aversive effects of drugs in self-administration: assessing the balance of reward and aversion in drug-taking behavior. Behav Pharmacol 24:363-74. doi: 10.1097/FBP.0b013e32836413d5
61. Vidal-Infer A, Arenas MC, Daza-Losada M, Aguilar MA, Miñarro J, Rodríguez-Arias M (2012) High novelty-seeking predicts greater sensitivity to the conditioned rewarding effects of cocaine. Pharmacol Biochem Behav 102:124-32. doi: 10.1016/j.pbb.2012.03.031
62. Wilcox RR (1987) New designs in analysis of variance. Annu Rev Psychol 38:29-60
63. Wittchen HU, Behrendt S, Höfler M, Perkonigg A, Lieb R, Bühringer G, Beesdo K (2008) What are the high risk periods for incident substance use and transitions to abuse and dependence? Implications for early intervention and prevention. Int J Methods Psychiatr Res 17:S16-29. doi: 10.1002/mpr.254
64. Zeelenberg R, Pecher D (2015) A method for simultaneously counterbalancing condition order and assignment of stimulus materials to conditions. Behav Res Methods 47(1):127-33. doi: 10.3758/s13428-014-0476-9