Binge ethanol drinking is an emerging pattern of excessive consumption among adolescents and young adults. Repeated ethanol intoxication has negative consequences during critical periods of brain development. Therefore, binge ethanol intake represents a vulnerability factor that promotes subsequent manifestations of neuropsychiatric disorders. In this study, we investigated the effects of oral binge ethanol intake during adolescence on the subsequent effects of cocaine in C57BL/6 mice. Firstly, we evaluated the oral ethanol intake of two binge ethanol procedures with different ethanol concentrations (20% v/v versus 30%, v/v). The highest ethanol intake was found in mice exposed to the lower ethanol concentration (20% v/v). In a second experiment, mice exposed to binge ethanol procedure were evaluated to study the effects of cocaine on locomotor activity, behavioural sensitization, and the reinforcing effects of cocaine in the self-administration paradigm. Mice exposed to ethanol binging showed discrete detrimental effects in responses to cocaine in the different experiments evaluated. Our findings revealed that the pattern of binge ethanol consumption in adolescent mice here evaluated produced a weak facilitation of cocaine responses. The present study highlights the importance of interventions to limit the deleterious effects of binge ethanol drinking during adolescence.
CaseyBJGlattCELeeFS (2015) Treating the developing versus developed brain: translating preclinical mouse and human studies. Neuron86: 1358–1368.
7.
Ciudad-RobertsACamarasaJCiudadCJ. (2015) Alcohol enhances the psychostimulant and conditioning effects of mephedrone in adolescent mice; postulation of unique roles of D3 receptors and BDNF in place preference acquisition. Br J Pharmacol172: 4970–4984.
8.
CrewsFTCollinsMADlugosC. (2004) Alcohol-induced neurodegeneration: when, where and why?Alcohol Clin Exp Res28: 350–364.
9.
CrewsFHeJHodgeC (2007) Adolescent cortical development: a critical period of vulnerability for addiction. Pharmacol Biochem Behav86: 189–199.
10.
CuthbertBN (2014) The RDoC framework: facilitating transition from ICD/DSM to dimensional approaches that integrates neuroscience and psychopathology. World Psychiatry13: 28–35.
11.
DeWitDJAdlafEMOffordDR. (2000) Age at first alcohol use: a risk factor for the development of alcohol disorders. Am J Psychiatry157: 745–750.
12.
Do CoutoBRRodríguez-AriasMFuentesS. (2011) Adolescent pre-exposure to ethanol or MDMA prolongs the conditioned rewarding effects of MDMA. Physiol Behav103: 585–593.
13.
DongYNestlerEJ (2014) The neural rejuvenation hypothesis of cocaine addiction. Trends Pharmacol Sci35: 374–83.
14.
EricksonCKByersKI (1989) Gastric contents alter blood alcohol levels and clearance after parenteral ethanol. Alcohol6: 249–252.
15.
EverittBJRobbinsTW (2016) Drug addiction: updating actions to habits to compulsions ten years on. Annu Rev Psychol67: 23–50.
16.
GieddJN (2008) The teen brain: insights from neuroimaging. J Adolesc Health42: 335–343.
17.
GirosBJaberMJonesSR. (1996) Hyperlocomotion and indifference to cocaine and amphetamine in mice lacking the dopamine transporter. Nature379: 606–612.
18.
Gracia-RubioIMoscoso-CastroMPozoOJ. (2016) Maternal separation induces neuroinflammation and long-lasting emotional alterations in mice. Prog Neuropsychopharmacol Biol Psychiatry65: 104–117.
19.
GuerriCPascualM (2010) Mechanisms involved in the neurotoxic, cognitive, and neurobehavioral effects of alcohol consumption during adolescence. Alcohol44: 15–26.
20.
HutchisonMARileyAL. (2012) Ethanol exposure during either adolescence or adulthood alters the rewarding effects of cocaine in adult rats. Pharmacol Biochem Behav101: 458–464.
21.
JohanssonEMGarcía-GutiérrezMSMoscoso-CastroM. (2015) Reduced contextual discrimination following alcohol consumption or MDMA administration in mice. PLoS One10: e0142978.
22.
MartinMLedentCParmentierM. (2000) Cocaine, but not morphine, induces conditioned place preference and sensitization to locomotor responses in CB1 knockout mice. Eur J Neurosci12: 4038–4046.
23.
MartiniMPintoAXValverdeO (2014) Estrous cycle and sex affect cocaine-induced behavioural changes in CD1 mice. Psychopharmacology231: 2647–2659.
24.
Mateos-GarcíaAManzanedoCRodríguez-AriasM. (2015) Sex differences in the long-lasting consequences of adolescent ethanol exposure for rewarding effects of cocaine in mice. Psychopharmacology232: 2995–3007.
25.
MoletJBouazizEHamonM. (2012) Early exposure to ethanol differentially affects ethanol preference at adult age in two inbred mouse strains. Neuropharmacology63: 338–348.
26.
MoletJHervéDThiébotMH. (2013) Juvenile ethanol exposure increases rewarding properties of cocaine and morphine in adult DBA/2J mice. Eur Neuropsychopharmacol23: 1816–1825.
27.
Navarro-ZaragozaJRos-SimóCMilanésMV. (2015) Binge ethanol and MDMA combination exacerbates toxic cardiac effects by inducing cellular stress. PLoS One10: e0141502.
28.
NybergF (2014) Structural plasticity of the brain to psychostimulant use. Neuropharmacology87: 115–124.
29.
OzburnARJanowskyAJCrabbeJC (2015) Commonalities and distinctions among mechanisms of addiction to alcohol and other drugs. Alcohol Clin Exp Res39: 1863–1877.
30.
PageyBDeeringDSellmanD (2010) Retention of adolescents with substance dependence and coexisting mental health disorders in outpatient alcohol and drug group therapy. Int J Ment Health Nurs19: 437–444.
31.
PascoliVTerrierJEspallerguesJ. (2014) Contrasting forms of cocaine-evoked plasticity control components of relapse. Nature509: 459–464.
32.
PascualMBoixJFelipoV. (2009) Repeated alcohol administration during adolescence causes changes in the mesolimbic dopaminergic and glutamatergic systems and promotes alcohol intake in the adult rat. J Neurochem108: 920–931.
33.
PascualMPlaAMiñarroJ. (2014) Neuroimmune activation and myelin changes in adolescent rats exposed to high-dose alcohol and associated cognitive dysfunction: a review with reference to human adolescent drinking. Alcohol Alcohol49: 187–192.
34.
PatelVChisholmDParikhR. (2016) Addressing the burden of mental, neurological, and substance use disorders: key messages from Disease Control Priorities. Lancet387: 1672–1685.
35.
PausTKeshavanMGieddJN (2008) Why do many psychiatric disorders emerge during adolescence?Nat Rev Neurosci9: 947–57.
36.
QuoilinC1DidoneVTirelliE. (2014) Higher long-lasting ethanol sensitization after adolescent ethanol exposure in mice. Psychopharmacology231: 1821–1829.
37.
RhodesJSBestKBelknapJK. (2005) Evaluation of a simple model of ethanol drinking to intoxication in C57BL/6J mice. Physiol Behav84: 53–63.
38.
RobinsonTEBerridgeKC (1993) The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Res Rev18: 247–291.
39.
Ros-SimóCRuiz-MedinaJValverdeO (2012) Behavioural and neuroinflammatory effects of the combination of binge ethanol and MDMA in mice. Psychopharmacology221: 511–525.
40.
Sanchez-RoigeSPeña-OliverYRipleyTL. (2014) Repeated ethanol exposure during early and late adolescence: double dissociation of effects on waiting and choice impulsivity. Alcohol Clin Exp Res38: 2579–2589.
41.
SlaweckiCJBetancourtMColeM. (2001) Periadolescent alcohol exposure has lasting effects on adult neurophysiological function in rats. Brain Res Dev Brain Res128: 63–72.
SpearLP (2000) The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev24: 417–463.
44.
SpearLP (2014) Adolescents and alcohol: acute sensitivities, enhanced intake, and later consequences. Neurotoxicol Teratol41: 51–59.
45.
SpearLP (2015) Adolescent alcohol exposure: are there separable vulnerable periods within adolescence?Physiol Behav148: 122–130.
46.
SpearLPSwartzwelderHS (2014) Adolescent alcohol exposure and persistence of adolescent-typical phenotypes into adulthood: a mini-review. Neurosci Biobehav Rev45: 1–8.
47.
SquegliaLMJacobusJTapertSF (2009) The influence of substance use on adolescent brain development. Clin EEG Neurosci40: 31–38.
48.
TaraziFIBaldessariniRJ (1999) Regional localization of dopamine and ionotropic glutamate receptor subtypes in striatolimbic brain regions. J Neurosci Res55: 401–410.
49.
TouriñoCValjentERuiz-MedinaJ. (2012) The orphan receptor GPR3 modulates the early phases of cocaine reinforcement. Br J Pharmacol167: 892–904.
50.
ValjentEBertran-GonzalezJAubierB. (2010) Mechanisms of locomotor sensitization to drugs of abuse in a two-injection protocol. Neuropsychopharmacology35: 401–415.
51.
VarlinskayaEIKimEUSpearLP (2016) Chronic intermittent ethanol exposure during adolescence: effects on stress-induced social alterations and social drinking in adulthood. Brain Res. Epub ahead of print 2Apr2016. DOI: 10.1016/j.brainres.2016.03.050.
52.
Vetter-O’HagenCSSpearLP (2012) The effects of gonadectomy on sex- and age-typical responses to novelty and ethanol-induced social inhibition in adult male and female Sprague-Dawley rats. Behav Brain Res227: 224–232.
53.
WDR-UNODC (2015) Global Status Report on Alcohol and Health. World Drug Report (UNODC).
54.
WechslerHNelsonTF (2001) Binge drinking and the American college student: what’s five drinks?Psychol Addict Behav15: 287–291.
55.
World Health Organization (WHO) (2014) Global status report on alcohol and health. Geneva: WHO, p. XIV.
56.
WoolvertonWLJohnsonKM (1992) Neurobiology of cocaine abuse. Trends Pharmacol Sci13: 193–200.
