Ethanol; Behavioral sensitization; Locomotor activity; Environmental enrichment; Social enrichment; Social isolation; Mice
Abstract :
[en] Rationale. In previous animal model studies, it was shown that drug sensitization is dependent upon physical environmental conditions. However, the effects of social housing conditions on drug sensitization is much less known.
Objective. The aim of the present study was to investigate the effects of social conditions, through the size of housing groups, on ethanol stimulant effects and ethanol-induced behavioral sensitization in mice.
Materials and methods. Male and female Swiss mice were housed in groups of different sizes (isolated mice, two mice per cage, four mice per cage and eight mice per cage) during a six-week period. A standard paradigm of ethanol-induced locomotor sensitization was then started with one daily injection of 2.5 g/kg ethanol for 8 consecutive days.
Results. The results show that social housing conditions affect the acute stimulant effects of ethanol. The highest stimulant effects were observed in socially isolated mice and then gradually decreased as the size of the group increased. Although the rate of ethanol sensitization did not differ between groups, the ultimate sensitized levels of ethanol-induced stimulant effects were significantly reduced in mice housed in groups of eight.
Conclusions. These results are consistent with the idea that higher levels of acute and sensitized ethanol stimulant effects are observed in mice housed in stressful housing conditions, such as social isolation. [fr] Contexte. Dans des études antérieures sur les modèles animaux, il a été démontré que la sensibilisation aux substances dépend des conditions environnementales physiques. Cependant, les effets des conditions d'hébergement social sur la sensibilisation aux drogues sont bien moins connus.
Objectif. L'objectif de la présente étude était d'explorer les effets des conditions sociales, à travers la taille des groupes d'hébergement , sur les effets stimulants de l'éthanol et la sensibilisation comportementale induite par l'éthanol chez la souris.
Matériel et méthodes. Des souris Swiss mâles et femelles ont été hébergées en groupes de tailles différentes (souris isolées, deux souris par cage, quatre souris par cage et huit souris par cage) pendant une période de six semaines. Un protocole standard de sensibilisation locomotrice induite par l'éthanol a ensuite été initié au moyen d'une injection quotidienne de 2,5 g/kg d'éthanol pendant 8 jours consécutifs.
Résultats. Les résultats démontrent que les conditions d'hébergement social affectent les effets stimulants aigus de l'éthanol. Les effets stimulants les plus élevés étaient observés chez les souris isolées socialement, puis diminuaient progressivement à mesure de l'augmentation de la taille du groupe. Bien que le taux de sensibilisation à l'éthanol ne différait pas entre les différents groupes, les niveaux de sensibilisation atteints des effets stimulants induits par l'éthanol étaient significativement réduits chez les souris hébergées en groupes de huit.
Conclusions. Ces résultats sont cohérents avec l'idée que des niveaux plus élevés d'effets stimulants aigus et sensibilisés induits par l'éthanol sont observés chez les souris hébergées dans des conditions de logement stressantes, comme l'isolement social.
Van Ingelgom, Théo ; Université de Liège - ULiège > Psychologie et Neuroscience Cognitives (PsyNCog) ; Université de Liège - ULiège > Département de Psychologie > Psychologie quantitative
Didone, Vincent ; Université de Liège - ULiège > Psychologie et Neuroscience Cognitives (PsyNCog) ; Université de Liège - ULiège > Département de Psychologie > Psychologie quantitative
Godefroid, Leeloo ; ULiège - Université de Liège [BE] > Psychologie et Neuroscience Cognitives (PsyNCog) > Département de Psychologie
Quertemont, Etienne ; Université de Liège - ULiège > Département de Psychologie > Psychologie quantitative ; Université de Liège - ULiège > Psychologie et Neuroscience Cognitives (PsyNCog)
Language :
English
Title :
Effects of social housing conditions on ethanol-induced behavioral sensitization in Swiss mice
Alternative titles :
[fr] Effets des conditions d'hébergement social sur la sensibilisation comportementale à l'éthanol chez la souris Swiss
Publication date :
11 January 2024
Journal title :
Psychopharmacology
ISSN :
0033-3158
eISSN :
1432-2072
Publisher :
Springer, Germany
Peer reviewed :
Peer Reviewed verified by ORBi
Name of the research project :
Effets de la manipulation de l’environnement social sur la vulnérabilité aux effets toxicomanogènes de l’alcool chez la souris
Funders :
ULiège. RISE - Université de Liège. Recherche, Innovation, Support et Entreprises [BE] ULiège FSR - Université de Liège. Fonds spéciaux pour la recherche [BE]
Funding text :
This work was supported by grants from the Recherche, Innovation, Support et Entreprises (RISE) from University
of Liège obtained by Théo van Ingelgom and the Fonds Spéciaux pour la Recherche de l’Université de Liège obtained by Etienne Quertetmont.
Akre AK, Bakken M, Hovland AL, Palme R, Mason G (2011) Clustered environmental enrichments induce more aggression and stereotypic behaviour than do dispersed enrichments in female mice. Appl Anim Behav Sci 131(3–4):145–152. 10.1016/j.applanim.2011.01.010 DOI: 10.1016/j.applanim.2011.01.010
Antelman SM, Eichler AJ, Black CA, Kocan D (1980) Interchangeability of stress and amphetamine in sensitization. Sci (New York N Y) 207(4428):329–331. 10.1126/science.7188649 DOI: 10.1126/science.7188649
Araujo NP, Camarini R, Souza-Formigoni MLO, Carvalho RC, Abílio VC, Silva RH, Ricardo VP, de Ribeiro R A., Frussa-Filho R (2005) The importance of housing conditions on behavioral sensitization and tolerance to ethanol. Pharmacol Biochem Behav 82(1):40–45. 10.1016/j.pbb.2005.07.009 DOI: 10.1016/j.pbb.2005.07.009
Araujo NP, Fukushiro DF, Cunha JLS, Levin R, Chinen CC, Carvalho RC, Ribeiro ICP, Gomes DC, Abílio VC, Silva RH, de Ribeiro R A., Frussa-Filho R (2006) Drug-induced home cage conspecifics’ behavior can potentiate behavioral sensitization in mice. Pharmacol Biochem Behav 84(1):142–147. 10.1016/j.pbb.2006.04.019 DOI: 10.1016/j.pbb.2006.04.019
Arndt SS, Laarakker MC, van Lith HA, van der Staay FJ, Gieling E, Salomons AR, van’t Klooster J, Ohl F (2009) Individual housing of mice—impact on behaviour and stress responses. Physiol Behav 97(3–4):385–393. 10.1016/j.physbeh.2009.03.008 DOI: 10.1016/j.physbeh.2009.03.008
Bahi A (2017) Environmental enrichment reduces chronic psychosocial stress-induced anxiety and ethanol-related behaviors in mice. Prog Neuropsychopharmacol Biol Psychiatry 77:65–74. 10.1016/j.pnpbp.2017.04.001 DOI: 10.1016/j.pnpbp.2017.04.001
Bahi A, Dreyer J-L (2020) Environmental enrichment decreases chronic psychosocial stress-impaired extinction and reinstatement of ethanol conditioned place preference in C57BL/6 male mice. Psychopharmacology 237(3):707–721. 10.1007/s00213-019-05408-8 DOI: 10.1007/s00213-019-05408-8
Bailoo JD, Murphy E, Boada-Saña M, Varholick JA, Hintze S, Baussière C, Hahn KC, Göpfert C, Palme R, Voelkl B, Würbel H (2018a) Effects of Cage Enrichment on Behavior, Welfare and Outcome Variability in Female mice. Front Behav Neurosci 12:232. 10.3389/fnbeh.2018.00232 DOI: 10.3389/fnbeh.2018.00232
Bailoo JD, Murphy E, Boada-Saña M, Varholick JA, Hintze S, Baussière C, Hahn KC, Göpfert C, Palme R, Voelkl B, Würbel H (2018b) Effects of Cage Enrichment on Behavior, Welfare and Outcome Variability in Female mice. Front Behav Neurosci 12:232. 10.3389/fnbeh.2018.00232 DOI: 10.3389/fnbeh.2018.00232
Barrera ED, Loughlin L, Greenberger S, Ewing S, Hachimine P, Ranaldi R (2021) Environmental enrichment reduces heroin seeking following incubation of craving in both male and female rats. Drug Alcohol Depend 226:108852. 10.1016/j.drugalcdep.2021.108852 DOI: 10.1016/j.drugalcdep.2021.108852
Bartolomucci A, Chirieleison A, Gioiosa L, Ceresini G, Parmigiani S, Palanza P (2004) Age at group formation alters behavior and physiology in male but not female CD-1 mice. Physiol Behav 82(2–3):425–434. 10.1016/j.physbeh.2004.04.011 DOI: 10.1016/j.physbeh.2004.04.011
Bartolomucci A, Palanza P, Sacerdote P, Panerai AE, Sgoifo A, Dantzer R, Parmigiani S (2005) Social factors and individual vulnerability to chronic stress exposure. Neurosci Biobehav Rev 29(1):67–81. 10.1016/j.neubiorev.2004.06.009 DOI: 10.1016/j.neubiorev.2004.06.009
Baumans V (2005) Environmental enrichment for laboratory rodents and rabbits: requirements of rodents, rabbits, and research. ILAR J 46(2):162–170. 10.1093/ilar.46.2.162 DOI: 10.1093/ilar.46.2.162
Baumans V, Van Loo PLP (2013) How to improve housing conditions of laboratory animals: the possibilities of environmental refinement. Vet J 195(1). 10.1016/j.tvjl.2012.09.023
Berardo LR, Fabio MC, Pautassi RM (2016) Post-weaning Environmental Enrichment, but not chronic maternal isolation, Enhanced Ethanol Intake during Periadolescence and early adulthood. Front Behav Neurosci 10. 10.3389/fnbeh.2016.00195
Berke JD, Hyman SE (2000) Addiction, dopamine, and the molecular mechanisms of memory. Neuron 25(3):515–532. 10.1016/s0896-6273(00)81056-9 DOI: 10.1016/s0896-6273(00)81056-9
Bisazza A (1981) Social organization and territorial behaviour in three strains of mice. Bolletino Di Zoologia 48(2):157–167. 10.1080/11250008109439329 DOI: 10.1080/11250008109439329
Broadbent J, Kampmueller KM, Koonse SA (2005) Role of dopamine in behavioral sensitization to ethanol in DBA/2J mice. Alcohol 35(2):137–148. 10.1016/j.alcohol.2005.03.006 DOI: 10.1016/j.alcohol.2005.03.006
Browman KE, Badiani A, Robinson TE (1998) Modulatory effect of environmental stimuli on the susceptibility to amphetamine sensitization: a dose-effect study in rats. J Pharmacol Exp Ther 287(3):1007–1014
Camarini R, Pautassi RM (2016) Behavioral sensitization to ethanol: neural basis and factors that influence its acquisition and expression. Brain Res Bull 125:53–78. 10.1016/j.brainresbull.2016.04.006 DOI: 10.1016/j.brainresbull.2016.04.006
Camarini R, Marcourakis T, Teodorov E, Yonamine M, Calil HM (2011) Ethanol-induced sensitization depends preferentially on D1 rather than D2 dopamine receptors. Pharmacol Biochem Behav 98(2):173–180. 10.1016/j.pbb.2010.12.017 DOI: 10.1016/j.pbb.2010.12.017
Camarini R, Marianno P, Rae M (2018) Social factors in ethanol sensitization. Int Rev Neurobiol 140:53–80. 10.1016/bs.irn.2018.07.003 DOI: 10.1016/bs.irn.2018.07.003
Chauvet C, Lardeux V, Goldberg SR, Jaber M, Solinas M (2009) Environmental enrichment reduces cocaine seeking and reinstatement induced by cues and stress but not by cocaine. Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology 34(13):2767–2778. 10.1038/npp.2009.127 DOI: 10.1038/npp.2009.127
Conrad KL, Winder DG (2011) Altered anxiety-like behavior and long-term potentiation in the bed nucleus of the stria terminalis in adult mice exposed to chronic social isolation, unpredictable stress, and ethanol beginning in adolescence. Alcohol 45(6). 10.1016/j.alcohol.2010.11.002
Cosgrove KP, Hunter RG, Carroll ME (2002) Wheel-running attenuates intravenous cocaine self-administration in rats: sex differences. Pharmacol Biochem Behav 73(3). https://doi.org/10.1016/s0091-3057(02)00853-5
Darlington TM, McCarthy RD, Cox RJ, Miyamoto-Ditmon J, Gallego X, Ehringer MA (2016) Voluntary wheel running reduces voluntary consumption of ethanol in mice: identification of candidate genes through striatal gene expression profiling. Genes Brain Behav 15(5). 10.1111/gbb.12294
Davis TA, Jovanovic T, Norrholm SD, Glover EM, Swanson M, Spann S, Bradley B (2013) Substance Use attenuates physiological responses Associated with PTSD among individuals with co-morbid PTSD and SUDs. J Psychol Psychother Suppl 7:006–. 10.4172/2161-0487.S7-006 DOI: 10.4172/2161-0487.S7-006
Deehan GA, Cain ME, Kiefer SW (2007) Differential rearing conditions alter operant responding for ethanol in outbred rats. Alcohol Clin Exp Res 31(10):1692–1698. 10.1111/j.1530-0277.2007.00466.x DOI: 10.1111/j.1530-0277.2007.00466.x
Deehan GA, Palmatier MI, Cain ME, Kiefer SW (2011) Differential rearing conditions and alcohol-preferring rats: consumption of and operant responding for ethanol. Behav Neurosci 125(2):184–193. 10.1037/a0022627 DOI: 10.1037/a0022627
Delaroque C, Chervy M, Gewirtz AT, Chassaing B (2021) Social overcrowding impacts gut microbiota, promoting stress, inflammation, and dysglycemia. Gut Microbes 13(1):2000275. 10.1080/19490976.2021.2000275 DOI: 10.1080/19490976.2021.2000275
Diamond MC (2001) Response of the brain to enrichment. Anais Da Academia Brasileira De Ciencias 73(2):211–220. 10.1590/s0001-37652001000200006 DOI: 10.1590/s0001-37652001000200006
Didone V, Quoilin C, Tirelli E, Quertemont E (2008) Parametric analysis of the development and expression of ethanol-induced behavioral sensitization in female Swiss mice: effects of dose, injection schedule, and test context. Psychopharmacology 201(2):249–260. 10.1007/s00213-008-1266-9 DOI: 10.1007/s00213-008-1266-9
Didone V, Masson S, Quoilin C, Seutin V, Quertemont E (2016) Correlation between ethanol behavioral sensitization and midbrain dopamine neuron reactivity to ethanol: ethanol sensitization. Addict Biol 21(2). https://doi.org/10.1111/adb.12216
Didone V, van Ingelgom T, Tirelli E, Quertemont E (2019) Long-term exposure to daily ethanol injections in DBA/2J and Swiss mice: lessons for the interpretation of ethanol sensitization. PLoS ONE 14(11):e0214696. 10.1371/journal.pone.0214696 DOI: 10.1371/journal.pone.0214696
Du Preez A, Onorato D, Eiben I, Musaelyan K, Egeland M, Zunszain PA, Fernandes C, Thuret S, Pariante CM (2021) Chronic stress followed by social isolation promotes depressive-like behaviour, alters microglial and astrocyte biology and reduces hippocampal neurogenesis in male mice. Brain Behav Immun 91:24–47. 10.1016/j.bbi.2020.07.015 DOI: 10.1016/j.bbi.2020.07.015
Edwards G, Arif A, Hadgson R (1981) Nomenclature and classification of drug- and alcohol-related problems: a WHO Memorandum. Bull World Health Organ 59(2):225–242
Farbstein D, Hollander N, Peled O, Apter A, Fennig S, Haberman Y, Gitman H, Yaniv I, Shkalim V, Pick CG, Benaroya-Milshtein N (2021) Social isolation in mice: Behavior, immunity, and tumor growth. Stress 24(2):229–238. 10.1080/10253890.2020.1777976 DOI: 10.1080/10253890.2020.1777976
Ferreira SEMM, Soares LM, Lira CR, Yokoyama TS, Engi SA, Cruz FC, Leão RM (2021) Ethanol-induced locomotor sensitization: neuronal activation in the nucleus accumbens and medial prefrontal cortex. Neurosci Lett 749:135745. 10.1016/j.neulet.2021.135745 DOI: 10.1016/j.neulet.2021.135745
Fish EW, DeBold JF, Miczek KA (2002) Repeated alcohol: behavioral sensitization and alcohol-heightened aggression in mice. Psychopharmacology 160(1):39–48. 10.1007/s00213-001-0934-9 DOI: 10.1007/s00213-001-0934-9
Fosnocht AQ, Lucerne KE, Ellis AS, Olimpo NA, Briand LA (2019) Adolescent social isolation increases cocaine seeking in male and female mice. Behav Brain Res 359:589–596. 10.1016/j.bbr.2018.10.007 DOI: 10.1016/j.bbr.2018.10.007
Fraser D (2009) Assessing animal welfare: different philosophies, different scientific approaches. Zoo Biol 28(6):507–518. 10.1002/zoo.20253 DOI: 10.1002/zoo.20253
Freese L, Almeida FB, Heidrich N, Hansen AW, Steffens L, Steinmetz A, Moura DJ, Gomez R, Barros HMT (2018) Environmental enrichment reduces cocaine neurotoxicity during cocaine-conditioned place preference in male rats. Pharmacol Biochem Behav 169:10–15. 10.1016/j.pbb.2018.04.001 DOI: 10.1016/j.pbb.2018.04.001
Galaj E, Manuszak M, Ranaldi R (2016) Environmental enrichment as a potential intervention for heroin seeking. Drug Alcohol Depend 163:195–201. 10.1016/j.drugalcdep.2016.04.016 DOI: 10.1016/j.drugalcdep.2016.04.016
Gamallo A, Villanua A, Trancho G, Fraile A (1986) Stress adaptation and adrenal activity in isolated and crowded rats. Physiol Behav 36(2):217–221. 10.1016/0031-9384(86)90006-5 DOI: 10.1016/0031-9384(86)90006-5
Garcia EJ, Haddon TN, Saucier DA, Cain ME (2017) Differential housing and novelty response: Protection and risk from locomotor sensitization. Pharmacol Biochem Behav 154:20–30. 10.1016/j.pbb.2017.01.004 DOI: 10.1016/j.pbb.2017.01.004
Geuzaine A, Tirelli E (2014) Wheel-running mitigates psychomotor sensitization initiation but not post-sensitization conditioned activity and conditioned place preference induced by cocaine in mice. Behav Brain Res 262:57–67. 10.1016/j.bbr.2014.01.002 DOI: 10.1016/j.bbr.2014.01.002
Greenough WT, Volkmar FR, Juraska JM (1973) Effects of rearing complexity on dendritic branching in frontolateral and temporal cortex of the rat. Exp Neurol 41(2):371–378. 10.1016/0014-4886(73)90278-1 DOI: 10.1016/0014-4886(73)90278-1
Haemisch A, Voss T, Gärtner K (1994) Effects of environmental enrichment on aggressive behavior, dominance hierarchies, and endocrine states in male DBA/2J mice. Physiol Behav 56(5):1041–1048. 10.1016/0031-9384(94)90341-7 DOI: 10.1016/0031-9384(94)90341-7
Hamilton KR, Elliott BM, Berger SS, Grunberg NE (2014) Environmental enrichment attenuates nicotine behavioral sensitization in male and female rats. Exp Clin Psychopharmacol 22(4):356–363. 10.1037/a0037205 DOI: 10.1037/a0037205
Hilakivi LA, Lister RG (1989) Effect of ethanol on the Social Behavior of Group-housed and isolated mice. Alcoholism: Clin Experimental Res 13(5). https://doi.org/10.1111/j.1530-0277.1989.tb00393.x
Hilakivi LA, Ota M, Lister RG (1989) Effect of isolation on brain monoamines and the behavior of mice in tests of exploration, locomotion, anxiety and behavioral « despair ». Pharmacol Biochem Behav 33(2):371–374. 10.1016/0091-3057(89)90516-9 DOI: 10.1016/0091-3057(89)90516-9
Holgate JY, Garcia H, Chatterjee S, Bartlett SE (2017) Social and environmental enrichment has different effects on ethanol and sucrose consumption in mice. Brain and Behavior 7(8). 10.1002/brb3.767
Imperio CG, McFalls AJ, Hadad N, Blanco-Berdugo L, Masser DR, Colechio EM, Coffey AA, Bixler GV, Stanford DR, Vrana KE, Grigson PS, Freeman WM (2018) Exposure to environmental enrichment attenuates addiction-like behavior and alters molecular effects of heroin self-administration in rats. Neuropharmacology 139:26–40. 10.1016/j.neuropharm.2018.06.037 DOI: 10.1016/j.neuropharm.2018.06.037
Kalivas PW, Stewart J (1991) Dopamine transmission in the initiation and expression of drug- and stress-induced sensitization of motor activity. Brain Res Rev 16(3):223–244. 10.1016/0165-0173(91)90007-U DOI: 10.1016/0165-0173(91)90007-U
Kappel S, Hawkins P, Mendl MT (2017a) To Group or not to Group? Good Practice for Housing Male Laboratory Mice. Animals: An Open Access Journal from MDPI 7(12). https://doi.org/10.3390/ani7120088
Kappel S, Hawkins P, Mendl MT (2017b) To Group or not to Group? Good Practice for Housing Male Laboratory Mice. Animals: An Open Access Journal from MDPI 7(12). https://doi.org/10.3390/ani7120088
Kawakami SE, Quadros IMH, Takahashi S, Suchecki D (2007) Long maternal separation accelerates behavioural sensitization to ethanol in female, but not in male mice. Behav Brain Res 184(2):109–116. 10.1016/j.bbr.2007.06.023 DOI: 10.1016/j.bbr.2007.06.023
Kawakami SE, Quadros IMH, Suchecki D (2016) Naltrexone prevents in males and attenuates in females the expression of behavioral sensitization to ethanol regardless of maternal separation. Front Endocrinol 7:135. 10.3389/fendo.2016.00135 DOI: 10.3389/fendo.2016.00135
Kempermann G (2019) Environmental enrichment, new neurons and the neurobiology of individuality. Nat Rev Neurosci 20(4):235–245. 10.1038/s41583-019-0120-x DOI: 10.1038/s41583-019-0120-x
Keyes KM, Hatzenbuehler ML, Hasin DS (2011) Stressful life experiences, alcohol consumption, and alcohol use disorders: the epidemiologic evidence for four main types of stressors. Psychopharmacology 218(1):1–17. 10.1007/s00213-011-2236-1 DOI: 10.1007/s00213-011-2236-1
Keyes KM, Hatzenbuehler ML, Grant BF, Hasin DS (2012) Stress and alcohol: epidemiologic evidence. Alcohol Research: Current Reviews 34(4):391–400
Khantzian EJ (2013) Addiction as a self-regulation disorder and the role of self-medication. Addiction (Abingdon England) 108(4):668–669. 10.1111/add.12004 DOI: 10.1111/add.12004
Kolb B, Gorny G, Söderpalm AHV, Robinson TE (2003) Environmental complexity has different effects on the structure of neurons in the prefrontal cortex versus the parietal cortex or nucleus accumbens. Synapse (New York N Y) 48(3):149–153. 10.1002/syn.10196 DOI: 10.1002/syn.10196
Komleva IK, Salmina AB, Prokopenko SV, Shestakova LA, Petrova MM, Malinovskaia NA, Lopatina OL (2013) [Changes in structural and functional plasticity of the brain induced by environmental enrichment]. Vestn Ross Akad Med Nauk 6:39–48. 10.15690/vramn.v68i6.672 DOI: 10.15690/vramn.v68i6.672
Koob GF, Volkow ND (2016) Neurobiology of addiction: a neurocircuitry analysis. The Lancet Psychiatry 3(8):760–773. 10.1016/S2215-0366(16)00104-8 DOI: 10.1016/S2215-0366(16)00104-8
Koob GF, Buck CL, Cohen A, Edwards S, Park PE, Schlosburg JE, Schmeichel B, Vendruscolo LF, Wade CL, Whitfield TW, George O (2014) Addiction as a stress surfeit disorder. Neuropharmacol 76 Pt B 370–382. https://doi.org/10.1016/j.neuropharm.2013.05.024
Kosten TR (2011) Stress and addiction. Am J Psychiatry 168(6):566–568. 10.1176/appi.ajp.2011.11020180 DOI: 10.1176/appi.ajp.2011.11020180
Kulesskaya N, Rauvala H, Voikar V (2011) Evaluation of Social and Physical Enrichment in Modulation of behavioural phenotype in C57BL/6J female mice. PLoS ONE 6(9):e24755. 10.1371/journal.pone.0024755 DOI: 10.1371/journal.pone.0024755
Landers MS, Knott GW, Lipp HP, Poletaeva I, Welker E (2011) Synapse formation in adult barrel cortex following naturalistic environmental enrichment. Neuroscience 199:143–152. 10.1016/j.neuroscience.2011.10.040 DOI: 10.1016/j.neuroscience.2011.10.040
Lazarus RS (1999) Stress and emotion: A new synthesis (p. xiv, 342). Springer Publishing Co
Legastelois R, Botia B, Coune F, Jeanblanc J, Naassila M (2014) Deciphering the relationship between vulnerability to ethanol-induced behavioral sensitization and ethanol consumption in outbred mice: EtOH sensitization and intake. Addict Biol 19(2):210–224. 10.1111/adb.12104 DOI: 10.1111/adb.12104
Lespine L-F, Tirelli E (2015) The protective effects of free wheel-running against cocaine psychomotor sensitization persist after exercise cessation in C57BL/6J mice. Neuroscience 310:650–664. 10.1016/j.neuroscience.2015.10.009 DOI: 10.1016/j.neuroscience.2015.10.009
Lespine L-F, Tirelli E (2018) Evidence for a long-term protection of wheel-running exercise against cocaine psychomotor sensitization in adolescent but not in adult mice. Behav Brain Res 349:63–72. 10.1016/j.bbr.2018.04.054 DOI: 10.1016/j.bbr.2018.04.054
Lin E-JD, Sun M, Choi EY, Magee D, Stets CW, During MJ (2015) Social overcrowding as a chronic stress model that increases adiposity in mice. Psychoneuroendocrinology 51:318–330. 10.1016/j.psyneuen.2014.10.007 DOI: 10.1016/j.psyneuen.2014.10.007
Lopez MF, Laber K (2015) Impact of social isolation and enriched environment during adolescence on voluntary ethanol intake and anxiety in C57BL/6J mice. Physiol Behav 148:151–156. 10.1016/j.physbeh.2014.11.012 DOI: 10.1016/j.physbeh.2014.11.012
Lynch WJ (2006) Sex differences in vulnerability to drug self-administration. Exp Clin Psychopharmacol 14(1):34–41. 10.1037/1064-1297.14.1.34 DOI: 10.1037/1064-1297.14.1.34
Lynch WJ, Piehl KB, Acosta G, Peterson AB, Hemby SE (2010) Aerobic Exercise attenuates reinstatement of Cocaine-seeking behavior and Associated neuroadaptations in the Prefrontal Cortex. Biol Psychiatry 68(8):774–777. 10.1016/j.biopsych.2010.06.022 DOI: 10.1016/j.biopsych.2010.06.022
Marashi V, Barnekow A, Sachser N (2004) Effects of environmental enrichment on males of a docile inbred strain of mice. Physiol Behav 82(5):765–776. 10.1016/j.physbeh.2004.05.009 DOI: 10.1016/j.physbeh.2004.05.009
Marianno P, Abrahao KP, Camarini R (2017) Environmental Enrichment Blunts Ethanol Consumption after Restraint stress in C57BL/6 mice. PLoS ONE 12(1). 10.1371/journal.pone.0170317
Masur J, Boerngen R (1980) The excitatory component of ethanol in mice: a chronic study. Pharmacol Biochem Behav 13(6). https://doi.org/10.1016/0091-3057(80)90206-3
Masur J, Oliveira de Souza ML, Zwicker AP (1986) The excitatory effect of ethanol: absence in rats, no tolerance and increased sensitivity in mice. Pharmacol Biochem Behav 24(5):1225–1228. 10.1016/0091-3057(86)90175-9 DOI: 10.1016/0091-3057(86)90175-9
Matonda-Ma-Nzuzi T, Didone V, Seutin V, Tirelli E, Quertemont E (2019) Investigating the reciprocal relationships between locomotor sensitization to ethanol and PTSD-like clusters in DBA/2J mice. Behav Brain Res 368:111909. 10.1016/j.bbr.2019.111909 DOI: 10.1016/j.bbr.2019.111909
Matsumoto K, Fujiwara H, Araki R, Yabe T (2019) Post-weaning social isolation of mice: a putative animal model of developmental disorders. J Pharmacol Sci 141(3):111–118. 10.1016/j.jphs.2019.10.002 DOI: 10.1016/j.jphs.2019.10.002
McCool BA, Chappell AM (2009) Early social isolation in male Long-Evans rats alters both appetitive and consummatory behaviors expressed during operant ethanol self-administration. Alcohol Clin Exp Res 33(2):273–282. 10.1111/j.1530-0277.2008.00830.x DOI: 10.1111/j.1530-0277.2008.00830.x
Mesa-Gresa P, Pérez-Martinez A, Redolat R (2013) Behavioral effects of combined environmental enrichment and chronic nicotine administration in male NMRI mice. Physiol Behav 114–115:65–76. 10.1016/j.physbeh.2013.03.010 DOI: 10.1016/j.physbeh.2013.03.010
Miczek KA, Barros HM, Sakoda L, Weerts EM (1998) Alcohol Clin Exp Res 22(8):1698–1705 DOI: 10.1111/j.1530-0277.1998.tb03968.x
Miczek KA, Maxson SC, Fish EW, Faccidomo S (2001) Aggressive behavioral phenotypes in mice. Behav Brain Res 125(1–2):167–181. 10.1016/s0166-4328(01)00298-4 DOI: 10.1016/s0166-4328(01)00298-4
Munn E, Bunning M, Prada S, Bohlen M, Crabbe JC, Wahlsten D (2011) Reversed light-dark cycle and cage enrichment effects on ethanol-induced deficits in motor coordination assessed in inbred mouse strains with a compact battery of refined tests. Behav Brain Res 224(2). 10.1016/j.bbr.2011.05.030
Nestler EJ (2001) Molecular basis of long-term plasticity underlying addiction. Nat Rev Neurosci 2(2):119–128. 10.1038/35053570 DOI: 10.1038/35053570
Newberry RC (1995) Environmental enrichment: increasing the biological relevance of captive environments. Appl Anim Behav Sci 44(2). https://doi.org/10.1016/0168-1591(95)00616-Z
O’Brien MA, Weston RM, Sheth NU, Bradley S, Bigbee J, Pandey A, Williams RW, Wolstenholme JT, Miles MF (2018) Ethanol-Induced behavioral sensitization alters the synaptic transcriptome and exon utilization in DBA/2J mice. Front Genet 9:402. 10.3389/fgene.2018.00402 DOI: 10.3389/fgene.2018.00402
Olsson IAS, Dahlborn K (2002a) Improving housing conditions for laboratory mice: a review of « environmental enrichment ». Lab Anim 36(3):243–270. 10.1258/002367702320162379 DOI: 10.1258/002367702320162379
Olsson IAS, Dahlborn K (2002b) Improving housing conditions for laboratory mice: a review of « environmental enrichment ». Lab Anim 36(3):243–270. 10.1258/002367702320162379 DOI: 10.1258/002367702320162379
Olsson IAS, Westlund K (2007a) More than numbers matter: the effect of social factors on behaviour and welfare of laboratory rodents and non-human primates. Appl Anim Behav Sci 103(3). https://doi.org/10.1016/j.applanim.2006.05.022
Olsson IAS, Westlund K (2007b) More than numbers matter: the effect of social factors on behaviour and welfare of laboratory rodents and non-human primates. Appl Anim Behav Sci 103(3):229–254. 10.1016/j.applanim.2006.05.022 DOI: 10.1016/j.applanim.2006.05.022
Olsson IAS, Westlund K (2007c) More than numbers matter: the effect of social factors on behaviour and welfare of laboratory rodents and non-human primates. Appl Anim Behav Sci 103(3):229–254. 10.1016/j.applanim.2006.05.022 DOI: 10.1016/j.applanim.2006.05.022
Olsson IAS, Nevison CM, Patterson-Kane EG, Sherwin CM, Van de Weerd HA, Würbel H (2003) Understanding behaviour: the relevance of ethological approaches in laboratory animal science. Appl Anim Behav Sci 81(3):245–264. 10.1016/S0168-1591(02)00285-X DOI: 10.1016/S0168-1591(02)00285-X
Päivärinta P (1990) Social isolation increases the stimulatory effect of ethanol on locomotor activity. Pharmacol Biochem Behav 36(2). https://doi.org/10.1016/0091-3057(90)90422-E
Powell GL, Vannan A, Bastle RM, Wilson MA, Dell’Orco M, Perrone-Bizzozero NI, Neisewander JL (2020) Environmental enrichment during forced abstinence from cocaine self-administration opposes gene network expression changes associated with the incubation effect. Sci Rep 10(1):11291. 10.1038/s41598-020-67966-8 DOI: 10.1038/s41598-020-67966-8
Quoilin C, Didone V, Tirelli E, Quertemont E (2012a) Chronic ethanol exposure during adolescence alters the behavioral responsiveness to ethanol in adult mice. Behav Brain Res 229(1):1–9. 10.1016/j.bbr.2011.12.039 DOI: 10.1016/j.bbr.2011.12.039
Quoilin C, Didone V, Tirelli E, Quertemont E (2012b) Developmental differences in ethanol-induced sensitization using postweanling, adolescent, and adult Swiss mice. 13
Quoilin C, Didone V, Tirelli E, Quertemont E (2014) Higher long-lasting ethanol sensitization after adolescent ethanol exposure in mice. Psychopharmacology 231(8) Article 8. https://doi.org/10.1007/s00213-013-3376-2
Robinson TE, Berridge KC (1993) The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Res Brain Res Rev 18(3):247–291. 10.1016/0165-0173(93)90013-p DOI: 10.1016/0165-0173(93)90013-p
Rodríguez-Ortega E, de la Fuente L, de Amo E, Cubero I (2018) Anxiety-Like, Novelty Seeking and Compulsive-Like Behaviors in C57BL/6J Mice During Adulthood. Front Behav Neurosci 12:177. 10.3389/fnbeh.2018.00177. Environmental Enrichment During Adolescence Acts as a Protective and Therapeutic Tool for Ethanol Binge-Drinking
Rosenzweig MR, Bennett EL (1972) Cerebral changes in rats exposed individually to an enriched environment. J Comp Physiological Psychol 80(2):304–313. 10.1037/h0032978 DOI: 10.1037/h0032978
Rueda AVL, Teixeira AMA, Yonamine M, Camarini R (2012) Environmental enrichment blocks ethanol-induced locomotor sensitization and decreases BDNF levels in the prefrontal cortex in mice: EE and ethanol sensitization. Addict Biol 17(4) Article 4. https://doi.org/10.1111/j.1369-1600.2011.00408.x
Sale A, Berardi N, Maffei L (2009) Enrich the environment to empower the brain. Trends Neurosci 32(4):233–239. 10.1016/j.tins.2008.12.004 DOI: 10.1016/j.tins.2008.12.004
Santos-Rocha JB, Rae M, Teixeira AMA, Teixeira SA, Munhoz CD, Muscará MN, Marcourakis T, Szumlinski KK, Camarini R (2018) Involvement of neuronal nitric oxide synthase in cross-sensitization between chronic unpredictable stress and ethanol in adolescent and adult mice. Alcohol 68:71–79. 10.1016/j.alcohol.2017.10.004 DOI: 10.1016/j.alcohol.2017.10.004
Sayette MA (1999) Does drinking reduce stress? Alcohol Res Health: J Natl Inst Alcohol Abuse Alcoholism 23(4):250–255
Scholz J, Allemang-Grand R, Dazai J, Lerch JP (2015) Environmental enrichment is associated with rapid volumetric brain changes in adult mice. NeuroImage 109:190–198. 10.1016/j.neuroimage.2015.01.027 DOI: 10.1016/j.neuroimage.2015.01.027
Schuhr B (1987) Social structure and plasma corticosterone level in female albino mice. Physiol Behav 40(6) Article 6. https://doi.org/10.1016/0031-9384(87)90269-1
Sikora M, Nicolas C, Istin M, Jaafari N, Thiriet N, Solinas M (2018) Generalization of effects of environmental enrichment on seeking for different classes of drugs of abuse. Behav Brain Res 341:109–113. 10.1016/j.bbr.2017.12.027 DOI: 10.1016/j.bbr.2017.12.027
Sinha R (2008) Chronic stress, drug use, and vulnerability to addiction. Ann N Y Acad Sci 1141:105–130. 10.1196/annals.1441.030 DOI: 10.1196/annals.1441.030
Sinha R (2009) Modeling stress and drug craving in the laboratory: implications for addiction treatment development. Addict Biol 14(1):84–98. 10.1111/j.1369-1600.2008.00134.x DOI: 10.1111/j.1369-1600.2008.00134.x
Smith MA, Schmidt KT, Iordanou JC, Mustroph ML (2008) Aerobic exercise decreases the positive-reinforcing effects of cocaine. Drug Alcohol Depend 98(1–2). https://doi.org/10.1016/j.drugalcdep.2008.05.006
Sofuoglu M, Rosenheck R, Petrakis I (2014) Pharmacological treatment of comorbid PTSD and substance use disorder: recent progress. Addict Behav 39(2):428–433. 10.1016/j.addbeh.2013.08.014 DOI: 10.1016/j.addbeh.2013.08.014
Solinas M, Chauvet C, Thiriet N, El Rawas R, Jaber M (2008) Reversal of cocaine addiction by environmental enrichment. Proc Natl Acad Sci USA 105(44):17145–17150. 10.1073/pnas.0806889105 DOI: 10.1073/pnas.0806889105
Solinas M, Thiriet N, Rawas RE, Lardeux V, Jaber M (2009) Environmental Enrichment during Early stages of Life reduces the behavioral, neurochemical, and Molecular effects of Cocaine. Neuropsychopharmacology 34(5). 10.1038/npp.2008.51
Stairs DJ, Ewin SE, Kangiser MM, Pfaff MN (2017) Effects of environmental enrichment on d-amphetamine self-administration following nicotine exposure. Exp Clin Psychopharmacol 25(5):393–401. 10.1037/pha0000137 DOI: 10.1037/pha0000137
Stevenson RA, Hoffman JL, Maldonado-Devincci AM, Faccidomo S, Hodge CW (2019) MGluR5 activity is required for the induction of ethanol behavioral sensitization and associated changes in ERK MAP kinase phosphorylation in the nucleus accumbens shell and lateral habenula. Behav Brain Res 367:19–27. 10.1016/j.bbr.2019.03.038 DOI: 10.1016/j.bbr.2019.03.038
Sullens DG, Gilley K, Jensen K, Vichaya E, Dolan SL, Sekeres MJ (2021) Social isolation induces hyperactivity and exploration in aged female mice. PLoS ONE 16(2):e0245355. 10.1371/journal.pone.0245355 DOI: 10.1371/journal.pone.0245355
Susser ER, Wallace RB (1982) The effects of environmental complexity on the hippocampal formation of the adult rat. Acta Neurobiol Exp 42(2):203–207
Sztainberg Y, Chen A (2010) An environmental enrichment model for mice. Nat Protoc 5(9) Article 9. https://doi.org/10.1038/nprot.2010.114
Valzelli L (1973) The « isolation syndrome » in mice. Psychopharmacologia 31(4):305–320. 10.1007/BF00421275 DOI: 10.1007/BF00421275
Van Loo PLP, de Groot AC, Van Zutphen BFM, Baumans V (2001) Do male mice prefer or avoid each other’s company? Influence of Hierarchy, Kinship, and Familiarity. J Appl Anim Welfare Sci 4(2):91–103. 10.1207/S15327604JAWS0402_1 DOI: 10.1207/S15327604JAWS0402_1
Van Loo PL, Mol JA, Koolhaas JM, Van Zutphen BF, Baumans V (2001a) Modulation of aggression in male mice: influence of group size and cage size. Physiol Behav 72(5):675–683. 10.1016/s0031-9384(01)00425-5 DOI: 10.1016/s0031-9384(01)00425-5
Van Loo PLP, Van Zutphen LFM, Baumans V (2003) Male management: coping with aggression problems in male laboratory mice. Lab Anim 37(4):300–313. 10.1258/002367703322389870 DOI: 10.1258/002367703322389870
Van Oortmerssen GA (1971) Biological significance, genetics and evolutionary origin of variability in behaviour within and between inbred strains of mice (Mus musculus). A behaviour genetic study. Behaviour 38(1):1–92. 10.1163/156853971x00014 DOI: 10.1163/156853971x00014
Vanderschuren LJMJ, Pierce RC (2010) Sensitization processes in drug addiction. Curr Top Behav Neurosci 3:179–195. 10.1007/7854_2009_21 DOI: 10.1007/7854_2009_21
Wojdala A, Molins F, Serrano MÁ (2020) Stress and drug addiction: an up-to-date perspective from 2020. Adicciones 32(4):239–242. 10.20882/adicciones.1470 DOI: 10.20882/adicciones.1470
Zlebnik NE, Anker JJ, Gliddon LA, Carroll ME (2010) Reduction of extinction and reinstatement of cocaine seeking by wheel running in female rats. Psychopharmacology 209(1):113–125. 10.1007/s00213-010-1776-0 DOI: 10.1007/s00213-010-1776-0