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
Volume :
241
Issue :
5
Pages :
987-1000
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 ULiège FSR - Université de Liège. Fonds spéciaux pour la recherche
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.
A.K. Akre M. Bakken A.L. Hovland R. Palme G. Mason Clustered environmental enrichments induce more aggression and stereotypic behaviour than do dispersed enrichments in female mice Appl Anim Behav Sci 2011 131 3–4 145 152 10.1016/j.applanim.2011.01.010
S.M. Antelman A.J. Eichler C.A. Black D. Kocan Interchangeability of stress and amphetamine in sensitization Sci (New York N Y) 1980 207 4428 329 331 1:CAS:528:DyaL3cXovVSrtQ%3D%3D 10.1126/science.7188649
N.P. Araujo R. Camarini M.L.O. Souza-Formigoni R.C. Carvalho V.C. Abílio R.H. Silva V.P. Ricardo R. de Ribeiro R. Frussa-Filho The importance of housing conditions on behavioral sensitization and tolerance to ethanol Pharmacol Biochem Behav 2005 82 1 40 45 1:CAS:528:DC%2BD2MXhtVyntL%2FP 10.1016/j.pbb.2005.07.009
N.P. Araujo D.F. Fukushiro J.L.S. Cunha R. Levin C.C. Chinen R.C. Carvalho I.C.P. Ribeiro D.C. Gomes V.C. Abílio R.H. Silva R. de Ribeiro R. Frussa-Filho Drug-induced home cage conspecifics’ behavior can potentiate behavioral sensitization in mice Pharmacol Biochem Behav 2006 84 1 142 147 1:CAS:528:DC%2BD28Xmslykurc%3D 10.1016/j.pbb.2006.04.019
S.S. Arndt M.C. Laarakker H.A. van Lith F.J. van der Staay E. Gieling A.R. Salomons J. van’t Klooster F. Ohl Individual housing of mice—impact on behaviour and stress responses Physiol Behav 2009 97 3–4 385 393 1:CAS:528:DC%2BD1MXmtFeqs7o%3D 10.1016/j.physbeh.2009.03.008
A. Bahi Environmental enrichment reduces chronic psychosocial stress-induced anxiety and ethanol-related behaviors in mice Prog Neuropsychopharmacol Biol Psychiatry 2017 77 65 74 1:CAS:528:DC%2BC2sXlvFygtbY%3D 10.1016/j.pnpbp.2017.04.001
A. Bahi J.-L. Dreyer Environmental enrichment decreases chronic psychosocial stress-impaired extinction and reinstatement of ethanol conditioned place preference in C57BL/6 male mice Psychopharmacology 2020 237 3 707 721 1:CAS:528:DC%2BC1MXit1Oiu7rJ 10.1007/s00213-019-05408-8
J.D. Bailoo E. Murphy M. Boada-Saña J.A. Varholick S. Hintze C. Baussière K.C. Hahn C. Göpfert R. Palme B. Voelkl H. Würbel Effects of Cage Enrichment on Behavior, Welfare and Outcome Variability in Female mice Front Behav Neurosci 2018 12 232 1:CAS:528:DC%2BC1MXitFWks7fJ 10.3389/fnbeh.2018.00232
J.D. Bailoo E. Murphy M. Boada-Saña J.A. Varholick S. Hintze C. Baussière K.C. Hahn C. Göpfert R. Palme B. Voelkl H. Würbel Effects of Cage Enrichment on Behavior, Welfare and Outcome Variability in Female mice Front Behav Neurosci 2018 12 232 1:CAS:528:DC%2BC1MXitFWks7fJ 10.3389/fnbeh.2018.00232
E.D. Barrera L. Loughlin S. Greenberger S. Ewing P. Hachimine R. Ranaldi Environmental enrichment reduces heroin seeking following incubation of craving in both male and female rats Drug Alcohol Depend 2021 226 108852 10.1016/j.drugalcdep.2021.108852
A. Bartolomucci A. Chirieleison L. Gioiosa G. Ceresini S. Parmigiani P. Palanza Age at group formation alters behavior and physiology in male but not female CD-1 mice Physiol Behav 2004 82 2–3 425 434 1:CAS:528:DC%2BD2cXmtVagu7s%3D 10.1016/j.physbeh.2004.04.011
A. Bartolomucci P. Palanza P. Sacerdote A.E. Panerai A. Sgoifo R. Dantzer S. Parmigiani Social factors and individual vulnerability to chronic stress exposure Neurosci Biobehav Rev 2005 29 1 67 81 10.1016/j.neubiorev.2004.06.009
V. Baumans Environmental enrichment for laboratory rodents and rabbits: requirements of rodents, rabbits, and research ILAR J 2005 46 2 162 170 1:CAS:528:DC%2BC3cXltVKmtg%3D%3D 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). https://doi.org/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. https://doi.org/10.3389/fnbeh.2016.00195
J.D. Berke S.E. Hyman Addiction, dopamine, and the molecular mechanisms of memory Neuron 2000 25 3 515 532 1:CAS:528:DC%2BD3cXisFKrtLw%3D 10.1016/s0896-6273(00)81056-9
A. Bisazza Social organization and territorial behaviour in three strains of mice Bolletino Di Zoologia 1981 48 2 157 167 10.1080/11250008109439329
J. Broadbent K.M. Kampmueller S.A. Koonse Role of dopamine in behavioral sensitization to ethanol in DBA/2J mice Alcohol 2005 35 2 137 148 1:CAS:528:DC%2BD2MXlt1WiurY%3D 10.1016/j.alcohol.2005.03.006
K.E. Browman A. Badiani T.E. Robinson Modulatory effect of environmental stimuli on the susceptibility to amphetamine sensitization: a dose-effect study in rats J Pharmacol Exp Ther 1998 287 3 1007 1014 1:CAS:528:DyaK1MXjvVSnsA%3D%3D
R. Camarini R.M. Pautassi Behavioral sensitization to ethanol: neural basis and factors that influence its acquisition and expression Brain Res Bull 2016 125 53 78 1:CAS:528:DC%2BC28XntVCnur4%3D 10.1016/j.brainresbull.2016.04.006
R. Camarini T. Marcourakis E. Teodorov M. Yonamine H.M. Calil Ethanol-induced sensitization depends preferentially on D1 rather than D2 dopamine receptors Pharmacol Biochem Behav 2011 98 2 173 180 1:CAS:528:DC%2BC3MXjsFGjurk%3D 10.1016/j.pbb.2010.12.017
R. Camarini P. Marianno M. Rae Social factors in ethanol sensitization Int Rev Neurobiol 2018 140 53 80 10.1016/bs.irn.2018.07.003
C. Chauvet V. Lardeux S.R. Goldberg M. Jaber M. Solinas 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 2009 34 13 2767 2778 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). https://doi.org/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). https://doi.org/10.1111/gbb.12294
T.A. Davis T. Jovanovic S.D. Norrholm E.M. Glover M. Swanson S. Spann B. Bradley Substance Use attenuates physiological responses Associated with PTSD among individuals with co-morbid PTSD and SUDs J Psychol Psychother 2013 7 006 10.4172/2161-0487.S7-006
G.A. Deehan M.E. Cain S.W. Kiefer Differential rearing conditions alter operant responding for ethanol in outbred rats Alcohol Clin Exp Res 2007 31 10 1692 1698 1:CAS:528:DC%2BD2sXht1KrtrvO 10.1111/j.1530-0277.2007.00466.x
G.A. Deehan M.I. Palmatier M.E. Cain S.W. Kiefer Differential rearing conditions and alcohol-preferring rats: consumption of and operant responding for ethanol Behav Neurosci 2011 125 2 184 193 1:CAS:528:DC%2BC3MXlslSqsbs%3D 10.1037/a0022627
C. Delaroque M. Chervy A.T. Gewirtz B. Chassaing Social overcrowding impacts gut microbiota, promoting stress, inflammation, and dysglycemia Gut Microbes 2021 13 1 2000275 10.1080/19490976.2021.2000275
M.C. Diamond Response of the brain to enrichment Anais Da Academia Brasileira De Ciencias 2001 73 2 211 220 1:STN:280:DC%2BD3MzjsF2huw%3D%3D 10.1590/s0001-37652001000200006
V. Didone C. Quoilin E. Tirelli E. Quertemont 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 2008 201 2 249 260 1:CAS:528:DC%2BD1cXhtlyjtL7K 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
V. Didone T. van Ingelgom E. Tirelli E. Quertemont Long-term exposure to daily ethanol injections in DBA/2J and Swiss mice: lessons for the interpretation of ethanol sensitization PLoS ONE 2019 14 11 e0214696 1:CAS:528:DC%2BC1MXit1ygs7rI 10.1371/journal.pone.0214696
A. Du Preez D. Onorato I. Eiben K. Musaelyan M. Egeland P.A. Zunszain C. Fernandes S. Thuret C.M. Pariante 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 2021 91 24 47 1:CAS:528:DC%2BB3cXitVSrtbbN 10.1016/j.bbi.2020.07.015
G. Edwards A. Arif R. Hadgson Nomenclature and classification of drug- and alcohol-related problems: a WHO Memorandum Bull World Health Organ 1981 59 2 225 242 1:STN:280:DyaL3M3jsVylsw%3D%3D
D. Farbstein N. Hollander O. Peled A. Apter S. Fennig Y. Haberman H. Gitman I. Yaniv V. Shkalim C.G. Pick N. Benaroya-Milshtein Social isolation in mice: Behavior, immunity, and tumor growth Stress 2021 24 2 229 238 1:CAS:528:DC%2BB3cXhsFSisbvM 10.1080/10253890.2020.1777976
S.E.M.M. Ferreira L.M. Soares C.R. Lira T.S. Yokoyama S.A. Engi F.C. Cruz R.M. Leão Ethanol-induced locomotor sensitization: neuronal activation in the nucleus accumbens and medial prefrontal cortex Neurosci Lett 2021 749 135745 1:CAS:528:DC%2BB3MXlsFSnsr0%3D 10.1016/j.neulet.2021.135745
E.W. Fish J.F. DeBold K.A. Miczek Repeated alcohol: behavioral sensitization and alcohol-heightened aggression in mice Psychopharmacology 2002 160 1 39 48 1:CAS:528:DC%2BD38XisVKlu7o%3D 10.1007/s00213-001-0934-9
A.Q. Fosnocht K.E. Lucerne A.S. Ellis N.A. Olimpo L.A. Briand Adolescent social isolation increases cocaine seeking in male and female mice Behav Brain Res 2019 359 589 596 1:CAS:528:DC%2BC1cXhvFSqurbL 10.1016/j.bbr.2018.10.007
D. Fraser Assessing animal welfare: different philosophies, different scientific approaches Zoo Biol 2009 28 6 507 518 10.1002/zoo.20253
L. Freese F.B. Almeida N. Heidrich A.W. Hansen L. Steffens A. Steinmetz D.J. Moura R. Gomez H.M.T. Barros Environmental enrichment reduces cocaine neurotoxicity during cocaine-conditioned place preference in male rats Pharmacol Biochem Behav 2018 169 10 15 1:CAS:528:DC%2BC1cXns1Srur0%3D 10.1016/j.pbb.2018.04.001
E. Galaj M. Manuszak R. Ranaldi Environmental enrichment as a potential intervention for heroin seeking Drug Alcohol Depend 2016 163 195 201 1:STN:280:DC%2BC28bktlKisg%3D%3D 10.1016/j.drugalcdep.2016.04.016
A. Gamallo A. Villanua G. Trancho A. Fraile Stress adaptation and adrenal activity in isolated and crowded rats Physiol Behav 1986 36 2 217 221 1:CAS:528:DyaL28Xht1egsbg%3D 10.1016/0031-9384(86)90006-5
E.J. Garcia T.N. Haddon D.A. Saucier M.E. Cain Differential housing and novelty response: Protection and risk from locomotor sensitization Pharmacol Biochem Behav 2017 154 20 30 1:CAS:528:DC%2BC2sXhsFGqu78%3D 10.1016/j.pbb.2017.01.004
A. Geuzaine E. Tirelli Wheel-running mitigates psychomotor sensitization initiation but not post-sensitization conditioned activity and conditioned place preference induced by cocaine in mice Behav Brain Res 2014 262 57 67 1:CAS:528:DC%2BC2cXisFCitL0%3D 10.1016/j.bbr.2014.01.002
W.T. Greenough F.R. Volkmar J.M. Juraska Effects of rearing complexity on dendritic branching in frontolateral and temporal cortex of the rat Exp Neurol 1973 41 2 371 378 1:STN:280:DyaE2c%2FhtlSmuw%3D%3D 10.1016/0014-4886(73)90278-1
A. Haemisch T. Voss K. Gärtner Effects of environmental enrichment on aggressive behavior, dominance hierarchies, and endocrine states in male DBA/2J mice Physiol Behav 1994 56 5 1041 1048 1:STN:280:DyaK2M7isFSgtQ%3D%3D 10.1016/0031-9384(94)90341-7
K.R. Hamilton B.M. Elliott S.S. Berger N.E. Grunberg Environmental enrichment attenuates nicotine behavioral sensitization in male and female rats Exp Clin Psychopharmacol 2014 22 4 356 363 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
L.A. Hilakivi M. Ota R.G. Lister Effect of isolation on brain monoamines and the behavior of mice in tests of exploration, locomotion, anxiety and behavioral « despair » Pharmacol Biochem Behav 1989 33 2 371 374 1:CAS:528:DyaL1MXls1OqsbY%3D 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). https://doi.org/10.1002/brb3.767
C.G. Imperio A.J. McFalls N. Hadad L. Blanco-Berdugo D.R. Masser E.M. Colechio A.A. Coffey G.V. Bixler D.R. Stanford K.E. Vrana P.S. Grigson W.M. Freeman Exposure to environmental enrichment attenuates addiction-like behavior and alters molecular effects of heroin self-administration in rats Neuropharmacology 2018 139 26 40 1:CAS:528:DC%2BC1cXht1yjurjF 10.1016/j.neuropharm.2018.06.037
P.W. Kalivas J. Stewart Dopamine transmission in the initiation and expression of drug- and stress-induced sensitization of motor activity Brain Res Rev 1991 16 3 223 244 1:CAS:528:DyaK38XhsVeqsLk%3D 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
S.E. Kawakami I.M.H. Quadros S. Takahashi D. Suchecki Long maternal separation accelerates behavioural sensitization to ethanol in female, but not in male mice Behav Brain Res 2007 184 2 109 116 1:CAS:528:DC%2BD2sXhtFeitLnE 10.1016/j.bbr.2007.06.023
S.E. Kawakami I.M.H. Quadros D. Suchecki Naltrexone prevents in males and attenuates in females the expression of behavioral sensitization to ethanol regardless of maternal separation Front Endocrinol 2016 7 135 10.3389/fendo.2016.00135
G. Kempermann Environmental enrichment, new neurons and the neurobiology of individuality Nat Rev Neurosci 2019 20 4 235 245 1:CAS:528:DC%2BC1MXmtFKhtbk%3D 10.1038/s41583-019-0120-x
K.M. Keyes M.L. Hatzenbuehler D.S. Hasin Stressful life experiences, alcohol consumption, and alcohol use disorders: the epidemiologic evidence for four main types of stressors Psychopharmacology 2011 218 1 1 17 1:CAS:528:DC%2BC3MXislCjtLk%3D 10.1007/s00213-011-2236-1
K.M. Keyes M.L. Hatzenbuehler B.F. Grant D.S. Hasin Stress and alcohol: epidemiologic evidence Alcohol Research: Current Reviews 2012 34 4 391 400 1:STN:280:DC%2BC3srltFOksg%3D%3D
E.J. Khantzian Addiction as a self-regulation disorder and the role of self-medication Addiction (Abingdon England) 2013 108 4 668 669 10.1111/add.12004
B. Kolb G. Gorny A.H.V. Söderpalm T.E. Robinson 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) 2003 48 3 149 153 1:CAS:528:DC%2BD3sXjt12rsL0%3D 10.1002/syn.10196
I.K. Komleva A.B. Salmina S.V. Prokopenko L.A. Shestakova M.M. Petrova N.A. Malinovskaia O.L. Lopatina [Changes in structural and functional plasticity of the brain induced by environmental enrichment] Vestn Ross Akad Med Nauk 2013 6 39 48 10.15690/vramn.v68i6.672
G.F. Koob N.D. Volkow Neurobiology of addiction: a neurocircuitry analysis The Lancet Psychiatry 2016 3 8 760 773 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
T.R. Kosten Stress and addiction Am J Psychiatry 2011 168 6 566 568 10.1176/appi.ajp.2011.11020180
N. Kulesskaya H. Rauvala V. Voikar Evaluation of Social and Physical Enrichment in Modulation of behavioural phenotype in C57BL/6J female mice PLoS ONE 2011 6 9 e24755 1:CAS:528:DC%2BC3MXht1ChsLjN 10.1371/journal.pone.0024755
M.S. Landers G.W. Knott H.P. Lipp I. Poletaeva E. Welker Synapse formation in adult barrel cortex following naturalistic environmental enrichment Neuroscience 2011 199 143 152 1:CAS:528:DC%2BC3MXhs1SgsL7K 10.1016/j.neuroscience.2011.10.040
Lazarus RS (1999) Stress and emotion: A new synthesis (p. xiv, 342). Springer Publishing Co
R. Legastelois B. Botia F. Coune J. Jeanblanc M. Naassila Deciphering the relationship between vulnerability to ethanol-induced behavioral sensitization and ethanol consumption in outbred mice: EtOH sensitization and intake Addict Biol 2014 19 2 210 224 1:CAS:528:DC%2BC2cXjt1Slurc%3D 10.1111/adb.12104
L.-F. Lespine E. Tirelli The protective effects of free wheel-running against cocaine psychomotor sensitization persist after exercise cessation in C57BL/6J mice Neuroscience 2015 310 650 664 1:CAS:528:DC%2BC2MXhs1CqurvK 10.1016/j.neuroscience.2015.10.009
L.-F. Lespine E. Tirelli Evidence for a long-term protection of wheel-running exercise against cocaine psychomotor sensitization in adolescent but not in adult mice Behav Brain Res 2018 349 63 72 1:CAS:528:DC%2BC1cXptFClur4%3D 10.1016/j.bbr.2018.04.054
E.-J.D. Lin M. Sun E.Y. Choi D. Magee C.W. Stets M.J. During Social overcrowding as a chronic stress model that increases adiposity in mice Psychoneuroendocrinology 2015 51 318 330 10.1016/j.psyneuen.2014.10.007
M.F. Lopez K. Laber Impact of social isolation and enriched environment during adolescence on voluntary ethanol intake and anxiety in C57BL/6J mice Physiol Behav 2015 148 151 156 1:CAS:528:DC%2BC2cXhvFegsLbM 10.1016/j.physbeh.2014.11.012
W.J. Lynch Sex differences in vulnerability to drug self-administration Exp Clin Psychopharmacol 2006 14 1 34 41 1:CAS:528:DC%2BD28XivVKktrs%3D 10.1037/1064-1297.14.1.34
W.J. Lynch K.B. Piehl G. Acosta A.B. Peterson S.E. Hemby Aerobic Exercise attenuates reinstatement of Cocaine-seeking behavior and Associated neuroadaptations in the Prefrontal Cortex Biol Psychiatry 2010 68 8 774 777 1:CAS:528:DC%2BC3cXht1ersrjJ 10.1016/j.biopsych.2010.06.022
V. Marashi A. Barnekow N. Sachser Effects of environmental enrichment on males of a docile inbred strain of mice Physiol Behav 2004 82 5 765 776 1:CAS:528:DC%2BD2cXnvFahtbw%3D 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). https://doi.org/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
J. Masur M.L. Oliveira de Souza A.P. Zwicker The excitatory effect of ethanol: absence in rats, no tolerance and increased sensitivity in mice Pharmacol Biochem Behav 1986 24 5 1225 1228 1:CAS:528:DyaL28XktlOgs7c%3D 10.1016/0091-3057(86)90175-9
T. Matonda-Ma-Nzuzi V. Didone V. Seutin E. Tirelli E. Quertemont Investigating the reciprocal relationships between locomotor sensitization to ethanol and PTSD-like clusters in DBA/2J mice Behav Brain Res 2019 368 111909 1:CAS:528:DC%2BC1MXosFSmsLs%3D 10.1016/j.bbr.2019.111909
K. Matsumoto H. Fujiwara R. Araki T. Yabe Post-weaning social isolation of mice: a putative animal model of developmental disorders J Pharmacol Sci 2019 141 3 111 118 1:CAS:528:DC%2BC1MXitVygsL%2FM 10.1016/j.jphs.2019.10.002
B.A. McCool A.M. Chappell Early social isolation in male Long-Evans rats alters both appetitive and consummatory behaviors expressed during operant ethanol self-administration Alcohol Clin Exp Res 2009 33 2 273 282 10.1111/j.1530-0277.2008.00830.x
P. Mesa-Gresa A. Pérez-Martinez R. Redolat Behavioral effects of combined environmental enrichment and chronic nicotine administration in male NMRI mice Physiol Behav 2013 114–115 65 76 1:CAS:528:DC%2BC3sXnt1Wrsro%3D 10.1016/j.physbeh.2013.03.010
K.A. Miczek H.M. Barros L. Sakoda E.M. Weerts Alcohol Clin Exp Res 1998 22 8 1698 1705 1:CAS:528:DyaK1cXnvFOiurs%3D 10.1111/j.1530-0277.1998.tb03968.x
K.A. Miczek S.C. Maxson E.W. Fish S. Faccidomo Aggressive behavioral phenotypes in mice Behav Brain Res 2001 125 1–2 167 181 1:STN:280:DC%2BD3MrnsVCqug%3D%3D 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). https://doi.org/10.1016/j.bbr.2011.05.030
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
M.A. O’Brien R.M. Weston N.U. Sheth S. Bradley J. Bigbee A. Pandey R.W. Williams J.T. Wolstenholme M.F. Miles Ethanol-Induced behavioral sensitization alters the synaptic transcriptome and exon utilization in DBA/2J mice Front Genet 2018 9 402 1:CAS:528:DC%2BC1MXpt1ait7Y%3D 10.3389/fgene.2018.00402
I.A.S. Olsson K. Dahlborn Improving housing conditions for laboratory mice: a review of « environmental enrichment » Lab Anim 2002 36 3 243 270 1:CAS:528:DC%2BD38XlslWisrg%3D 10.1258/002367702320162379
I.A.S. Olsson K. Dahlborn Improving housing conditions for laboratory mice: a review of « environmental enrichment » Lab Anim 2002 36 3 243 270 1:CAS:528:DC%2BD38XlslWisrg%3D 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
I.A.S. Olsson K. Westlund More than numbers matter: the effect of social factors on behaviour and welfare of laboratory rodents and non-human primates Appl Anim Behav Sci 2007 103 3 229 254 10.1016/j.applanim.2006.05.022
I.A.S. Olsson K. Westlund More than numbers matter: the effect of social factors on behaviour and welfare of laboratory rodents and non-human primates Appl Anim Behav Sci 2007 103 3 229 254 10.1016/j.applanim.2006.05.022
I.A.S. Olsson C.M. Nevison E.G. Patterson-Kane C.M. Sherwin H.A. Van de Weerd H. Würbel Understanding behaviour: the relevance of ethological approaches in laboratory animal science Appl Anim Behav Sci 2003 81 3 245 264 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
G.L. Powell A. Vannan R.M. Bastle M.A. Wilson M. Dell’Orco N.I. Perrone-Bizzozero J.L. Neisewander Environmental enrichment during forced abstinence from cocaine self-administration opposes gene network expression changes associated with the incubation effect Sci Rep 2020 10 1 11291 1:CAS:528:DC%2BB3cXhtlyju7vL 10.1038/s41598-020-67966-8
C. Quoilin V. Didone E. Tirelli E. Quertemont Chronic ethanol exposure during adolescence alters the behavioral responsiveness to ethanol in adult mice Behav Brain Res 2012 229 1 1 9 1:CAS:528:DC%2BC38Xjs1agsL4%3D 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
T.E. Robinson K.C. Berridge The neural basis of drug craving: an incentive-sensitization theory of addiction Brain Res Brain Res Rev 1993 18 3 247 291 1:CAS:528:DyaK3sXlsFWnu78%3D 10.1016/0165-0173(93)90013-p
E. Rodríguez-Ortega L. de la Fuente E. de Amo I. Cubero Environmental Enrichment During Adolescence Acts as a Protective and Therapeutic Tool for Ethanol Binge-Drinking 2018 10.3389/fnbeh.2018.00177
M.R. Rosenzweig E.L. Bennett Cerebral changes in rats exposed individually to an enriched environment J Comp Physiological Psychol 1972 80 2 304 313 1:STN:280:DyaE383ktlamug%3D%3D 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
A. Sale N. Berardi L. Maffei Enrich the environment to empower the brain Trends Neurosci 2009 32 4 233 239 1:CAS:528:DC%2BD1MXkt1SktL8%3D 10.1016/j.tins.2008.12.004
J.B. Santos-Rocha M. Rae A.M.A. Teixeira S.A. Teixeira C.D. Munhoz M.N. Muscará T. Marcourakis K.K. Szumlinski R. Camarini Involvement of neuronal nitric oxide synthase in cross-sensitization between chronic unpredictable stress and ethanol in adolescent and adult mice Alcohol 2018 68 71 79 1:CAS:528:DC%2BC1cXkslSiur8%3D 10.1016/j.alcohol.2017.10.004
M.A. Sayette Does drinking reduce stress? Alcohol Res Health: J Natl Inst Alcohol Abuse Alcoholism 1999 23 4 250 255 1:STN:280:DC%2BD3czpsVSgtA%3D%3D
J. Scholz R. Allemang-Grand J. Dazai J.P. Lerch Environmental enrichment is associated with rapid volumetric brain changes in adult mice NeuroImage 2015 109 190 198 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
M. Sikora C. Nicolas M. Istin N. Jaafari N. Thiriet M. Solinas Generalization of effects of environmental enrichment on seeking for different classes of drugs of abuse Behav Brain Res 2018 341 109 113 10.1016/j.bbr.2017.12.027
R. Sinha Chronic stress, drug use, and vulnerability to addiction Ann N Y Acad Sci 2008 1141 105 130 1:CAS:528:DC%2BD1cXhsVOkt7bP 10.1196/annals.1441.030
R. Sinha Modeling stress and drug craving in the laboratory: implications for addiction treatment development Addict Biol 2009 14 1 84 98 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
M. Sofuoglu R. Rosenheck I. Petrakis Pharmacological treatment of comorbid PTSD and substance use disorder: recent progress Addict Behav 2014 39 2 428 433 10.1016/j.addbeh.2013.08.014
M. Solinas C. Chauvet N. Thiriet R. El Rawas M. Jaber Reversal of cocaine addiction by environmental enrichment Proc Natl Acad Sci USA 2008 105 44 17145 17150 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). https://doi.org/10.1038/npp.2008.51
D.J. Stairs S.E. Ewin M.M. Kangiser M.N. Pfaff Effects of environmental enrichment on d-amphetamine self-administration following nicotine exposure Exp Clin Psychopharmacol 2017 25 5 393 401 1:CAS:528:DC%2BC1MXitVOkurfK 10.1037/pha0000137
R.A. Stevenson J.L. Hoffman A.M. Maldonado-Devincci S. Faccidomo C.W. Hodge 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 2019 367 19 27 1:CAS:528:DC%2BC1MXmsVWhtLg%3D 10.1016/j.bbr.2019.03.038
D.G. Sullens K. Gilley K. Jensen E. Vichaya S.L. Dolan M.J. Sekeres Social isolation induces hyperactivity and exploration in aged female mice PLoS ONE 2021 16 2 e0245355 1:CAS:528:DC%2BB3MXjs1eis7w%3D 10.1371/journal.pone.0245355
E.R. Susser R.B. Wallace The effects of environmental complexity on the hippocampal formation of the adult rat Acta Neurobiol Exp 1982 42 2 203 207 1:STN:280:DyaL3s7nsV2ntQ%3D%3D
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
L. Valzelli The « isolation syndrome » in mice Psychopharmacologia 1973 31 4 305 320 1:STN:280:DyaE2c%2Fgt1Oktw%3D%3D 10.1007/BF00421275
P.L.P. Van Loo A.C. de Groot B.F.M. Van Zutphen V. Baumans Do male mice prefer or avoid each other’s company? Influence of Hierarchy, Kinship, and Familiarity J Appl Anim Welfare Sci 2001 4 2 91 103 10.1207/S15327604JAWS0402_1
P.L. Van Loo J.A. Mol J.M. Koolhaas B.F. Van Zutphen V. Baumans Modulation of aggression in male mice: influence of group size and cage size Physiol Behav 2001 72 5 675 683 10.1016/s0031-9384(01)00425-5
P.L.P. Van Loo L.F.M. Van Zutphen V. Baumans Male management: coping with aggression problems in male laboratory mice Lab Anim 2003 37 4 300 313 10.1258/002367703322389870
G.A. Van Oortmerssen Biological significance, genetics and evolutionary origin of variability in behaviour within and between inbred strains of mice (Mus musculus). A behaviour genetic study Behaviour 1971 38 1 1 92 10.1163/156853971x00014
L.J.M.J. Vanderschuren R.C. Pierce Sensitization processes in drug addiction Curr Top Behav Neurosci 2010 3 179 195 10.1007/7854_2009_21
A. Wojdala F. Molins M.Á. Serrano Stress and drug addiction: an up-to-date perspective from 2020 Adicciones 2020 32 4 239 242 10.20882/adicciones.1470
N.E. Zlebnik J.J. Anker L.A. Gliddon M.E. Carroll Reduction of extinction and reinstatement of cocaine seeking by wheel running in female rats Psychopharmacology 2010 209 1 113 125 1:CAS:528:DC%2BC3cXht1amsrg%3D 10.1007/s00213-010-1776-0
