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Alcohol, psychomotor-stimulants and behaviour: methodological considerations in preclinical models of early-life stress

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Abstract

Background

In order to assess the risk associated with early-life stress, there has been an increase in the amount of preclinical studies investigating early-life stress. There are many challenges associated with investigating early-life stress in animal models and ensuring that such models are appropriate and clinically relevant.

Objectives

The purpose of this review is to highlight the methodological considerations in the design of preclinical studies investigating the effects of early-life stress on alcohol and psychomotor-stimulant intake and behaviour.

Methods

The protocols employed for exploring early-life stress were investigated and summarised. Experimental variables include animals, stress models, and endpoints employed.

Results

The findings in this paper suggest that there is little consistency among these studies and so the interpretation of these results may not be as clinically relevant as previously thought.

Conclusion

The standardisation of these simple stress procedures means that results will be more comparable between studies and that results generated will give us a more robust understanding of what can and may be happening in the human and veterinary clinic.

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Abbreviations

SD:

Sprague-Dawley

L-E:

Long-Evans

L-H:

Lister Hooded

F-H:

Fawn-Hooded

Cont:

Continuous

NS:

Not specified

PND:

Postnatal day

M:

Male

F:

Female

CPP:

Conditioned place preference

AMP:

Amphetamine

MA:

Methamphetamine

2-BC:

2 Bottle-choice

MDMA:

Methylenedioxymethamnphetamine

CVS:

Chronic variable stress

AA:

Alko alcohol

ANA:

Alko non-alcohol

OSST:

Operant strategy-shifting task

SI:

Social interaction

EPM:

Elevated plus maze

OFT:

Open field test

FST:

Forced swim test

LDB:

Light/dark box

LA:

Locomotor activity

MWM:

Morris water maze

cPRIDE:

Consummatory partial reinforcement on incentive downshift effect

AST:

Attention set-shifting task

ASR:

Acoustic startle response

CMS:

Chronic-mild-unpredictable stress

TMT:

Trimethylthiazoline

SUS:

Swim-test susceptible

RES:

Swim-test resistant

NOR:

Novel object recognition

PCMS:

Predictable chronic mild stress

NSFT:

Novelty-suppressed feeding test

RHA:

Roman high avoidance

RLA:

Roman low avoidance

PPI:

Prepulse inhibition

SP:

Sucrose/saccharin preference

FC:

Fear conditioning

RI:

Resident-intruder

Interm:

Intermittent

EE:

Environmental enrichment

MS:

Maternal separation

CORT:

Corticosterone

F2:

Second generation

References

  • Abelaira HM, Reus GZ, Quevedo J (2013) Animal models as tools to study the pathophysiology of depression. Revista Brasileira de Psiquiatria 35:S112–S120

    Article  PubMed  Google Scholar 

  • Acevedo MB, Pautassi RM, Spear NE, Spear LP (2013) Age-dependent effects of stress on ethanol-induced motor activity in rats. Psychopharmacology (Berl) 230:389–398

    Article  CAS  Google Scholar 

  • Advani T, Hensler JG, Koek W (2007) Effect of early rearing conditions on alcohol drinking and 5-HT1A receptor function in C57BL/6J mice. Int J Neuropsychopharmacol 10:595–607

    Article  CAS  PubMed  Google Scholar 

  • Amiri S, Haj-mirzaian A, Rahimi-balaei M, Razmi A, Kordjazy N, Shirzadian A, Ejtemaei Mehr S, Sianati H, Dehpour AR (2015) Co-occurrence of anxiety and depressive-like behaviors following adolescent social isolation in male mice; possible role of nitrergic system. Physiol Behav 145:38–44

    Article  CAS  PubMed  Google Scholar 

  • Andersen SL, Thompson AT, Rutstein M, Hostetter JC, Teicher MH (2000) Dopamine receptor pruning in prefrontal cortex during the periadolescent period in rats. Synapse 37:167–169

    Article  CAS  PubMed  Google Scholar 

  • Anderson RI, Varlinskaya EI, Spear LP (2010) Ethanol-induced conditioned taste aversion in male Sprague-Dawley rats: impact of age and stress. Alcohol Clin Exp Res 34:2106–2115

    Article  PubMed  PubMed Central  Google Scholar 

  • Anker JJ, Carroll ME (2010) Reinstatement of cocaine seeking induced by drugs, cues, and stress in adolescent and adult rats. Psychopharmacology (Berl) 208:211–222

    Article  CAS  Google Scholar 

  • Ariza Traslavina GA, de Oliveira FL, Franci CR (2014) Early adolescent stress alters behavior and the HPA axis response in male and female adult rats: the relevance of the nature and duration of the stressor. Physiol Behav 133:178–189

    Article  PubMed  CAS  Google Scholar 

  • Auger AP, Olesen KM (2009) Brain sex differences and the organization of juvenile social play behavior. J Neuroendocrinol 21:519–525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baarendse PJ, Limpens JH, Vanderschuren LJ (2014) Disrupted social development enhances the motivation for cocaine in rats. Psychopharmacology (Berl) 231:1695–1704

    Article  CAS  Google Scholar 

  • Becker HC, Lopez MF, Doremus-Fitzwater TL (2011) Effects of stress on alcohol drinking: a review of animal studies. Psychopharmacology 218(1):131–156

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bell HC, MC Caffrey DR, Forgie ML, Kolb B, Pellis SM (2009) The role of the medial prefrontal cortex in the play fighting of rats. Behav Neurosci 123:1158–1168

    Article  PubMed  Google Scholar 

  • Bell HC, Pellis SM, Kolb B (2010) Juvenile peer play experience and the development of the orbitofrontal and medial prefrontal cortices. Behav Brain Res 207:7–13

    Article  PubMed  Google Scholar 

  • Bingham B, MC Fadden K, Zhang X, Bhatnagar S, Beck S, Valentino R (2011) Early adolescence as a critical window during which social stress distinctly alters behavior and brain norepinephrine activity. Neuropsychopharmacology 36:896–909

    Article  CAS  PubMed  Google Scholar 

  • Bourke CH, Neigh GN (2011) Behavioral effects of chronic adolescent stress are sustained and sexually dimorphic. Horm Behav 60:112–120

    Article  PubMed  PubMed Central  Google Scholar 

  • Brielmaier J, Mc Donald CG, Smith RF (2012) Effects of acute stress on acquisition of nicotine conditioned place preference in adolescent rats: a role for corticotropin-releasing factor 1 receptors. Psychopharmacology (Berl) 219:73–82

    Article  CAS  Google Scholar 

  • Brunell SC, Spear LP (2005) Effect of stress on the voluntary intake of a sweetened ethanol solution in pair-housed adolescent and adult rats. Alcohol Clin Exp Res 29:1641–1653

    Article  PubMed  Google Scholar 

  • Burke AR, Forster GL, Novick AM, Roberts CL, Watt MJ (2013) Effects of adolescent social defeat on adult amphetamine-induced locomotion and corticoaccumbal dopamine release in male rats. Neuropharmacology 67:359–369

    Article  CAS  PubMed  Google Scholar 

  • Burke AR, Miczek KA (2014) Stress in adolescence and drugs of abuse in rodent models: role of dopamine, CRF, and HPA axis. Psychopharmacology (Berl) 231:1557–1580

    Article  CAS  Google Scholar 

  • Burke AR, Miczek KA (2015) Escalation of cocaine self-administration in adulthood after social defeat of adolescent rats: role of social experience and adaptive coping behavior. Psychopharmacology (Berl) 232:3067–3079

    Article  CAS  Google Scholar 

  • Burke AR, Renner KJ, Forster GL, Watt MJ (2010) Adolescent social defeat alters neural, endocrine and behavioral responses to amphetamine in adult male rats. Brain Res 1352:147–156

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burke AR, Watt MJ, Forster GL (2011) Adolescent social defeat increases adult amphetamine conditioned place preference and alters D2 dopamine receptor expression. Neuroscience 197:269–279

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Butkevich IP, Mikhailenko VA, Vershinina EA, ULANOVA NA (2015) Differences in adaptive behaviors in adolescent male and female rats exposed as newborns to inflammatory pain or stress. Zh Evol Biokhim Fiziol 51:266–275

    CAS  PubMed  Google Scholar 

  • Butler TR, Carter E, Weiner JL (2014) Adolescent social isolation does not lead to persistent increases in anxiety-like behavior or ethanol intake in female long-evans rats. Alcohol Clin Exp Res 38:2199–2207

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buwalda B, Geerdink M, Vidal J, Koolhaas JM (2011) Social behavior and social stress in adolescence: a focus on animal models. Neurosci Biobehav Rev 35:1713–1721

    Article  PubMed  Google Scholar 

  • Buwalda B, Stubbendorff C, Zickert N, Koolhaas JM (2013) Adolescent social stress does not necessarily lead to a compromised adaptive capacity during adulthood: a study on the consequences of social stress in rats. Neuroscience 249:258–270

    Article  CAS  PubMed  Google Scholar 

  • Callaghan BL, Richardson R (2012) Early-life stress affects extinction during critical periods of development: an analysis of the effects of maternal separation on extinction in adolescent rats. Stress 15:671–679

    Article  PubMed  Google Scholar 

  • Cao X, Huang S, Cao J, Chen T, Zhu P, Zhu R, Su P, Ruan D (2014) The timing of maternal separation affects morris water maze performance and long-term potentiation in male rats. Dev Psychobiol 56:1102–1109

    Article  PubMed  Google Scholar 

  • Chaby LE, Sheriff MJ, Hirrlinger AM, Lim J, Fetherston TB, Braithwaite VA (2015) Does chronic unpredictable stress during adolescence affect spatial cognition in adulthood? PLoS One 10:e0141908

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Charney DS, Heninger GR, Redmond DE, JR. (1983) Yohimbine induced anxiety and increased noradrenergic function in humans: effects of diazepam and clonidine. Life Sci 33:19–29

    Article  CAS  PubMed  Google Scholar 

  • Chattarji S, Tomar A, Suvrathan A, Ghosh S, Rahman MM (2015) Neighborhood matters: divergent patterns of stress-induced plasticity across the brain. Nat Neurosci 18:1364–1375

    Article  CAS  PubMed  Google Scholar 

  • Chester JA, Barrenha GD, Hughes ML, Keuneke KJ (2008) Age- and sex-dependent effects of footshock stress on subsequent alcohol drinking and acoustic startle behavior in mice selectively bred for high-alcohol preference. Alcohol Clin Exp Res 32:1782–1794

    Article  PubMed  PubMed Central  Google Scholar 

  • Chocyk A, Majcher-Maslanka I, Przyborowska A, Mackowiak M, Wedzony K (2015) Early-life stress increases the survival of midbrain neurons during postnatal development and enhances reward-related and anxiolytic-like behaviors in a sex-dependent fashion. Int J Dev Neurosci 44:33–47

    Article  PubMed  Google Scholar 

  • Chocyk A, Przyborowska A, Makuch W, Majcher-Maslanka I, Dudys D, Wedzony K (2014) The effects of early-life adversity on fear memories in adolescent rats and their persistence into adulthood. Behav Brain Res 264:161–172

    Article  PubMed  Google Scholar 

  • Choy KH, Van den Buuse M (2008) Attenuated disruption of prepulse inhibition by dopaminergic stimulation after maternal deprivation and adolescent corticosterone treatment in rats. Eur Neuropsychopharmacol 18:1–13

    Article  CAS  PubMed  Google Scholar 

  • Collins TF, Sprando RL, Shackelford ME, Hansen DK, Welsh JJ (1999) Food and Drug Administration proposed testing guidelines for reproduction studies. Revision Committee. FDA Guidelines for Developmental Toxicity and Reproduction, Food and Drug Administration. Regul Toxicol Pharmacol 30:29–38

    Article  CAS  PubMed  Google Scholar 

  • 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 45:585–593

    Article  CAS  PubMed  Google Scholar 

  • Coppens CM, Coolen A, de Boer SF, Koolhaas JM (2014) Adolescent social defeat disturbs adult aggression-related impulsivity in wild-type rats. Behav Processes 108:191–196

    Article  PubMed  Google Scholar 

  • Coppens CM, de Boer SF, Steimer T, Koolhaas JM (2012) Impulsivity and aggressive behavior in Roman high and low avoidance rats: baseline differences and adolescent social stress induced changes. Physiol Behav 105:1156–1160

    Article  CAS  PubMed  Google Scholar 

  • Cordero MI, Ansermet F, Sandi C (2013) Long-term programming of enhanced aggression by peripuberty stress in female rats. Psychoneuroendocrinology 38:2758–2769

    Article  PubMed  Google Scholar 

  • Covington HE 3rd, Miczek KA (2001) Repeated social-defeat stress, cocaine or morphine. Effects on behavioral sensitization and intravenous cocaine self-administration “binges”. Psychopharmacology (Berl) 158:388–398

    Article  CAS  Google Scholar 

  • Cruz FC, Delucia R, Planeta CS (2008a) Effects of chronic stress on nicotine-induced locomotor activity and corticosterone release in adult and adolescent rats. Addict Biol 13:63–69

    Article  CAS  PubMed  Google Scholar 

  • Cruz FC, Marin MT, Leao RM, Planeta CS (2012) Behavioral and neuroendocrine effects of the exposure to chronic restraint or variable stress in early adolescent rats. Int J Dev Neurosci 30:19–23

    Article  CAS  PubMed  Google Scholar 

  • Cruz FC, Quadros IM, da Planeta CS, Miczek KA (2008b) Maternal separation stress in male mice: long-term increases in alcohol intake. Psychopharmacology (Berl) 201:459–468

    Article  CAS  Google Scholar 

  • Cuenya L, Mustaca A, Kamenetzky G (2015) Postweaning isolation affects responses to incentive contrast in adulthood. Dev Psychobiol 57:177–188

    Article  PubMed  Google Scholar 

  • Cumming MJ, Thompson MA, MC Cormick CM (2014) Adolescent social instability stress increases aggression in a food competition task in adult male Long-Evans rats. Dev Psychobiol 56:1575–1588

    Article  PubMed  Google Scholar 

  • Daston G, Faustman E, Ginsberg G, Fenner-Crisp P, Olin S, Sonawane B, Bruckner J, Breslin W, MC Laughlin TJ (2004) A framework for assessing risks to children from exposure to environmental agents. Environ Health Perspect 112:238–256

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Davis M, Redmond DEJR, Baraban JM (1979) Noradrenergic agonists and antagonists: effects on conditioned fear as measured by the potentiated startle paradigm. Psychopharmacology (Berl) 65:111–118

    Article  CAS  Google Scholar 

  • Dayi A, Cetin F, Sisman AR, Aksu I, Tas A, Gonenc S, Uysal N (2015) The effects of oxytocin on cognitive defect caused by chronic restraint stress applied to adolescent rats and on hippocampal VEGF and BDNF levels. Med Sci Monit 21:69–75

    Article  PubMed  PubMed Central  Google Scholar 

  • Deehan GAJR, Cain ME, Kiefer SW (2007) Differential rearing conditions alter operant responding for ethanol in outbred rats. Alcohol Clin Exp Res 31:1692–1698

    Article  CAS  PubMed  Google Scholar 

  • Ding Y, Kang L, Li B, Ma L (2005) Enhanced cocaine self-administration in adult rats with adolescent isolation experience. Pharmacol Biochem Behav 82:673–677

    Article  CAS  Google Scholar 

  • do Prado CH, Narahari T, Holland FH, Lee HN, Murthy SK, Brenhouse HC (2016) Effects of early adolescent environmental enrichment on cognitive dysfunction, prefrontal cortex development, and inflammatory cytokines after early life stress. Dev Psychobiol 58:482–491

    Article  CAS  PubMed  Google Scholar 

  • Dong M, Anda RF, Felitti VJ, Dube SR, Williamson DF, Thompson TJ, Loo CM, Giles WH (2004) The interrelatedness of multiple forms of childhood abuse, neglect, and household dysfunction. Child Abuse Negl 28:771–784

    Article  PubMed  Google Scholar 

  • Doremus-Fitzwater TL, Varlinskaya EI, Spear LP (2009) Social and non-social anxiety in adolescent and adult rats after repeated restraint. Physiol Behav 97:484–494

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Douglas LA, Varlinskaya EI, Spear LP (2003) Novel-object place conditioning in adolescent and adult male and female rats: effects of social isolation. Physiol Behav 80:317–325

    Article  CAS  PubMed  Google Scholar 

  • Ehlers CL, Walker BM, Pian JP, Roth JL, Slawecki CJ (2007) Increased alcohol drinking in isolate-housed alcohol-preferring rats. Behav Neurosci 121:111–119

    Article  PubMed  Google Scholar 

  • Enoch MA (2006) Genetic and environmental influences on the development of alcoholism: resilience vs. risk. Ann N Y Acad Sci 1094:193–201

    Article  PubMed  Google Scholar 

  • Enoch MA (2011) The role of early life stress as a predictor for alcohol and drug dependence. Psychopharmacology (Berl) 214:17–31

    Article  CAS  Google Scholar 

  • Fahlke C, Hard E, Eriksson CJ (1997) Effects of early weaning and social isolation on subsequent alcohol intake in rats. Alcohol 14:175–180

    Article  CAS  PubMed  Google Scholar 

  • Feltenstein MW, See RE (2006) Potentiation of cue-induced reinstatement of cocaine-seeking in rats by the anxiogenic drug yohimbine. Behav Brain Res 174:1–8

    Article  CAS  PubMed  Google Scholar 

  • Ferris CF, Brewer J (1996) Adolescent stress alters ethanol ingestion and agonistic behavior in the male golden hamster. Ann N Y Acad Sci 794:348–351

    Article  CAS  PubMed  Google Scholar 

  • Francis DD, Meaney MJ (1999) Maternal care and the development of stress responses. Current Opinion in Neurobiology 9:128–134

    Article  CAS  PubMed  Google Scholar 

  • Freund N, Thompson BS, Denormandie J, Vaccarro K, Andersen SL (2013) Windows of vulnerability: maternal separation, age, and fluoxetine on adolescent depressive-like behavior in rats. Neuroscience 249:88–97

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Furuta M, Ninomiya-Baba M, Chiba S, Funabashi T, Akema T, Kunugi H (2015) Exposure to social defeat stress in adolescence improves the working memory and anxiety-like behavior of adult female rats with intrauterine growth restriction, independently of hippocampal neurogenesis. Horm Behav 70:30–37

    Article  PubMed  Google Scholar 

  • Gan JO, Bowline E, Lourenco FS, Pickel VM (2014) Adolescent social isolation enhances the plasmalemmal density of NMDA NR1 subunits in dendritic spines of principal neurons in the basolateral amygdala of adult mice. Neuroscience 258:174–183

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Pardo MP, Blanco-Gandia MC, Valiente-Lluch M, Rodriguez-Arias M, Minarro J, Aguilar MA (2015) Long-term effects of repeated social stress on the conditioned place preference induced by MDMA in mice. Prog Neuropsychopharmacol Biol Psychiatry 63:98–109

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Pardo MP, Rodriguez-Arias M, Maldonado C, Manzanedo C, Minarro J, Aguilar MA (2014) Effects of acute social stress on the conditioned place preference induced by MDMA in adolescent and adult mice. Behav Pharmacol 25:532–546

    CAS  PubMed  Google Scholar 

  • Girotti M, Pace TW, Gaylord RI, Rubin BA, Herman JP, Spencer RL (2006) Habituation to repeated restraint stress is associated with lack of stress-induced c-fos expression in primary sensory processing areas of the rat brain. Neuroscience 138:1067–1081

    Article  CAS  PubMed  Google Scholar 

  • Goldman L, Winget C, Hollingshead GW, Levine S (1973) Postweaning development of negative feedback in the pituitary-adrenal system of the rat. Neuroendocrinology 12:199–211

    Article  CAS  PubMed  Google Scholar 

  • Green JG, Mc Laughlin KA, Berglund PA, Gruber MJ, Sampson NA, Zaslavsky AM, Kessler RC (2010) Childhood adversities and adult psychiatric disorders in the national comorbidity survey replication I: associations with first onset of DSM-IV disorders. Arch Gen Psychiatry 67:113–123

    Article  PubMed  PubMed Central  Google Scholar 

  • Green MR, Mc Cormick CM (2013a) Effects of social instability stress in adolescence on long-term, not short-term, spatial memory performance. Behav Brain Res 256:165–171

    Article  PubMed  Google Scholar 

  • Green MR, Mc Cormick CM (2013b) Effects of stressors in adolescence on learning and memory in rodent models. Horm Behav 64:364–379

    Article  PubMed  Google Scholar 

  • Gruss M, Braun K, Frey JU, Korz V (2008) Maternal separation during a specific postnatal time window prevents reinforcement of hippocampal long-term potentiation in adolescent rats. Neuroscience 152:1–7

    Article  CAS  PubMed  Google Scholar 

  • Guo M, Wu CF, Liu W, Yang JY, Chen D (2004) Sex difference in psychological behavior changes induced by long-term social isolation in mice. Prog Neuropsychopharmacol Biol Psychiatry 28:115–121

    Article  PubMed  Google Scholar 

  • Hall FS, Huang S, Fong GW, Pert A, Linnoila M (1998) Effects of isolation-rearing on voluntary consumption of ethanol, sucrose and saccharin solutions in Fawn Hooded and Wistar rats. Psychopharmacology (Berl) 139:210–216

    Article  CAS  Google Scholar 

  • Hancock SD, Menard JL, Olmstead MC (2005) Variations in maternal care influence vulnerability to stress-induced binge eating in female rats. Physiol Behav 85:430–439

    Article  CAS  PubMed  Google Scholar 

  • Handy C, Yanaga S, Reiss A, Zona N, Robinson E, Saxton KB (2016) Stress during adolescence alters palatable food consumption in a context-dependent manner. PLoS One 11:e0148261

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Harrell CS, Hardy E, Boss-Williams K, Weiss JM, Neigh GN (2013) Sex and lineage interact to predict behavioral effects of chronic adolescent stress in rats. Behav Brain Res 248:57–61

    Article  PubMed  PubMed Central  Google Scholar 

  • Hensleigh E, Smedley L, Pritchard LM (2011) Sex, but not repeated maternal separation during the first postnatal week, influences novel object exploration and amphetamine sensitivity. Dev Psychobiol 53:132–140

    Article  CAS  PubMed  Google Scholar 

  • Himmler, B. T., Pellis, V. C. & Pellis, S. M. 2013. Peering into the dynamics of social interactions: measuring play fighting in rats. J Vis Exp.

  • Hodges TE, Mc Cormick CM (2015) Adolescent and adult male rats habituate to repeated isolation, but only adolescents sensitize to partner unfamiliarity. Horm Behav 69:16–30

    Article  PubMed  Google Scholar 

  • Hong S, Flashner B, Chiu M, Ver Hoeve E, Luz S, Bhatnagar S (2012) Social isolation in adolescence alters behaviors in the forced swim and sucrose preference tests in female but not in male rats. Physiol Behav 105:269–275

    Article  CAS  PubMed  Google Scholar 

  • Howes SR, Dalley JW, Morrison CH, Robbins TW, Everitt BJ (2000) Leftward shift in the acquisition of cocaine self-administration in isolation-reared rats: relationship to extracellular levels of dopamine, serotonin and glutamate in the nucleus accumbens and amygdala-striatal FOS expression. Psychopharmacology (Berl) 151:55–63

    Article  CAS  Google Scholar 

  • Huang GB, Zhao T, Muna SS, Bagalkot TR, Jin HM, Chae HJ, Chung YC (2013) Effects of chronic social defeat stress on behaviour, endoplasmic reticulum proteins and choline acetyltransferase in adolescent mice. Int J Neuropsychopharmacol 16:1635–1647

    Article  CAS  PubMed  Google Scholar 

  • Huot RL, Thrivikraman KV, Meaney MJ, Plotsky PM (2001) Development of adult ethanol preference and anxiety as a consequence of neonatal maternal separation in Long Evans rats and reversal with antidepressant treatment. Psychopharmacology (Berl) 158:366–373

    Article  CAS  Google Scholar 

  • Iniguez SD, Riggs LM, Nieto SJ, Dayrit G, Zamora NN, Shawhan KL, Cruz B, Warren BL (2014) Social defeat stress induces a depression-like phenotype in adolescent male c57BL/6 mice. Stress 17:247–255

    Article  PubMed  PubMed Central  Google Scholar 

  • Isgor C, Kabbaj M, Akil H, Watson SJ (2004) Delayed effects of chronic variable stress during peripubertal-juvenile period on hippocampal morphology and on cognitive and stress axis functions in rats. Hippocampus 14:636–648

    Article  PubMed  Google Scholar 

  • Joseph A, Tang M, Mamiya T, Chen Q, Yang LL, Jiao J, Yu N, Tang YP (2013) Temporal association of elevated cholecystokininergic tone and adolescent trauma is critical for posttraumatic stress disorder-like behavior in adult mice. Proc Natl Acad Sci U S A 110:6589–6594

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Juarez J, Vazquez-Cortes C (2003) Alcohol intake in social housing and in isolation before puberty and its effects on voluntary alcohol consumption in adulthood. Dev Psychobiol 43:200–207

    Article  PubMed  Google Scholar 

  • Juvonen J, Graham S, Schuster MA (2003) Bullying among young adolescents: the strong, the weak, and the troubled. Pediatrics 112:1231–1237

    Article  PubMed  Google Scholar 

  • Kabbaj M, Isgor C, Watson SJ, Akil H (2002) Stress during adolescence alters behavioral sensitization to amphetamine. Neuroscience 113:395–400

    Article  CAS  PubMed  Google Scholar 

  • Kaffman A, Meaney MJ (2007) Neurodevelopmental sequelae of postnatal maternal care in rodents: clinical and research implications of molecular insights. Journal of Child Psychology and Psychiatry 48:224–244

    Article  PubMed  Google Scholar 

  • Karkhanis AN, Alexander NJ, Mc Cool BA, Weiner JL, Jones SR (2015) Chronic social isolation during adolescence augments catecholamine response to acute ethanol in the basolateral amygdala. Synapse 69:385–395

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kendig MD, Bowen MT, Kemp AH, Mc Gregor IS (2011) Predatory threat induces huddling in adolescent rats and residual changes in early adulthood suggestive of increased resilience. Behav Brain Res 225:405–414

    Article  PubMed  Google Scholar 

  • Kercmar J, Budefeld T, Grgurevic N, Tobet SA, Majdic G (2011) Adolescent social isolation changes social recognition in adult mice. Behav Brain Res 216:647–651

    Article  PubMed  Google Scholar 

  • Khoshbouei H, Cecchi M, Dove S, Javors M, Morilak DA (2002) Behavioral reactivity to stress: amplification of stress-induced noradrenergic activation elicits a galanin-mediated anxiolytic effect in central amygdala. Pharmacol Biochem Behav 71:407–417

    Article  CAS  PubMed  Google Scholar 

  • Klein ZA, Padow VA, Romeo RD (2010) The effects of stress on play and home cage behaviors in adolescent male rats. Dev Psychobiol 52:62–70

    PubMed  Google Scholar 

  • Koehnle TJ, Rinaman L (2010) Early experience alters limbic forebrain Fos responses to a stressful interoceptive stimulus in young adult rats. Physiol Behav 100:105–115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kornetsky C (1989) Animal models: promises and problems. In: Koob GF, Ehlers CL, Kupfer DJ (eds) Animal models of depression. Boston, Birkhäuser Boston

    Google Scholar 

  • Kovalenko IL, Galyamina AG, Smagin DA, Michurina TV, Kudryavtseva NN, Enikolopov G (2014) Extended effect of chronic social defeat stress in childhood on behaviors in adulthood. PLoS One 9:e91762

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kubala KH, Christianson JP, Kaufman RD, Watkins LR, Maier SF (2012) Short- and long-term consequences of stressor controllability in adolescent rats. Behav Brain Res 234:278–284

    Article  PubMed  PubMed Central  Google Scholar 

  • Lancaster FE (1998) Sex differences in voluntary drinking by Long Evans rats following early stress. Alcohol Clin Exp Res 22:830–836

    Article  CAS  PubMed  Google Scholar 

  • Lariviere WR, Sattar MA, Melzack R (2006) Inflammation-susceptible Lewis rats show less sensitivity than resistant Fischer rats in the formalin inflammatory pain test and with repeated thermal testing. J Neurophysiol 95:2889–2897

    Article  PubMed  Google Scholar 

  • Lee H, Noh J (2015) Social exclusion intensifies anxiety-like behavior in adolescent rats. Behav Brain Res 284:112–117

    Article  PubMed  Google Scholar 

  • Lepsch LB, Gonzalo LA, Magro FJ, Delucia R, Scavone C, Planeta CS (2005) Exposure to chronic stress increases the locomotor response to cocaine and the basal levels of corticosterone in adolescent rats. Addict Biol 10:251–256

    Article  CAS  PubMed  Google Scholar 

  • Levine S (1957) Infantile experience and resistance to physiological stress. Science 126:405

    Article  CAS  PubMed  Google Scholar 

  • LEVINE S, LEWIS GW (1959) Critical period for effects of infantile experience on maturation of stress response. Science 129:42–43

    Article  CAS  PubMed  Google Scholar 

  • Lewis EM, JR BJF, Freshwater L, Hoberman AM, Christian MS (2002) Sexual maturation data for Crl Sprague-Dawley rats: criteria and confounding factors. Drug Chem Toxicol 25:437–458

    Article  CAS  PubMed  Google Scholar 

  • Li C, Liu Y, Liu D, Jiang H, Pan F (2016) Dynamic alterations of miR-34c expression in the hypothalamus of male rats after early adolescent traumatic stress. Neural Plast 2016:5249893

    PubMed  PubMed Central  Google Scholar 

  • Li C, Liu Y, Yin S, Lu C, Liu D, Jiang H, Pan F (2015) Long-term effects of early adolescent stress: dysregulation of hypothalamic-pituitary-adrenal axis and central corticotropin releasing factor receptor 1 expression in adult male rats. Behav Brain Res 288:39–49

    Article  CAS  PubMed  Google Scholar 

  • Llorente-Berzal A, Fuentes S, Gagliano H, Lopez-Gallardo M, Armario A, Viveros MP, Nadal R (2011) Sex-dependent effects of maternal deprivation and adolescent cannabinoid treatment on adult rat behaviour. Addict Biol 16:624–637

    Article  CAS  PubMed  Google Scholar 

  • Llorente-Berzal A, Manzanedo C, Daza-Losada M, Valero M, Lopez-Gallardo M, Aguilar MA, Rodriguez-Arias M, Minarro J, Viveros MP (2013) Sex-dependent effects of early maternal deprivation on MDMA-induced conditioned place preference in adolescent rats: possible neurochemical correlates. Toxicology 311:78–86

    Article  CAS  PubMed  Google Scholar 

  • Llorente-Berzal A, Mela V, Borcel E, Valero M, Lopez-Gallardo M, Viveros MP, Marco EM (2012) Neurobehavioral and metabolic long-term consequences of neonatal maternal deprivation stress and adolescent olanzapine treatment in male and female rats. Neuropharmacology 62:1332–1341

    Article  CAS  PubMed  Google Scholar 

  • Llorente R, Arranz L, Marco EM, Moreno E, Puerto M, Guaza C, de la Fuente M, Viveros MP (2007) Early maternal deprivation and neonatal single administration with a cannabinoid agonist induce long-term sex-dependent psychoimmunoendocrine effects in adolescent rats. Psychoneuroendocrinology 32:636–650

    Article  CAS  PubMed  Google Scholar 

  • Lodge DJ, Lawrence AJ (2003) The CRF1 receptor antagonist antalarmin reduces volitional ethanol consumption in isolation-reared fawn-hooded rats. Neuroscience 117:243–247

    Article  CAS  PubMed  Google Scholar 

  • Lopez MF, Doremus-Fitzwater TL, Becker HC (2011) Chronic social isolation and chronic variable stress during early development induce later elevated ethanol intake in adult C57BL/6J mice. Alcohol 45:355–364

    Article  CAS  PubMed  Google Scholar 

  • Lukkes JL, Mokin MV, Scholl JL, Forster GL (2009) Adult rats exposed to early-life social isolation exhibit increased anxiety and conditioned fear behavior, and altered hormonal stress responses. Horm Behav 55:248–256

    Article  CAS  PubMed  Google Scholar 

  • Luo XM, Yuan SN, Guan XT, Xie X, Shao F, Wang WW (2014) Juvenile stress affects anxiety-like behavior and limbic monoamines in adult rats. Physiol Behav 135:7–16

    Article  CAS  PubMed  Google Scholar 

  • Lyttle K, Ohmura Y, Konno K, Yoshida T, Izumi T, Watanabe M, Yoshioka M (2015) Repeated fluvoxamine treatment recovers juvenile stress-induced morphological changes and depressive-like behavior in rats. Brain Res 1616:88–100

    Article  CAS  PubMed  Google Scholar 

  • Marco EM, Valero M, de la Serna O, Aisa B, Borcel E, Ramirez MJ, VIVEROS MP (2013) Maternal deprivation effects on brain plasticity and recognition memory in adolescent male and female rats. Neuropharmacology 68:223–231

    Article  CAS  PubMed  Google Scholar 

  • Marin MT, Planeta CS (2004) Maternal separation affects cocaine-induced locomotion and response to novelty in adolescent, but not in adult rats. Brain Res 1013:83–90

    Article  CAS  PubMed  Google Scholar 

  • Marquardt AR, Ortiz-Lemos L, Lucion AB, Barros HM (2004) Influence of handling or aversive stimulation during rats' neonatal or adolescence periods on oral cocaine self-administration and cocaine withdrawal. Behav Pharmacol 15:403–412

    Article  CAS  PubMed  Google Scholar 

  • Martini M, Valverde O (2012) A single episode of maternal deprivation impairs the motivation for cocaine in adolescent mice. Psychopharmacology (Berl) 219:149–158

    Article  CAS  Google Scholar 

  • Mathews IZ, Mills RG, Mc Cormick CM (2008a) Chronic social stress in adolescence influenced both amphetamine conditioned place preference and locomotor sensitization. Dev Psychobiol 50:451–459

    Article  CAS  PubMed  Google Scholar 

  • Mathews IZ, Wilton A, Styles A, Mc Cormick CM (2008b) Increased depressive behaviour in females and heightened corticosterone release in males to swim stress after adolescent social stress in rats. Behav Brain Res 190:33–40

    Article  CAS  PubMed  Google Scholar 

  • Mc Cool 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 33:273–282

    Article  Google Scholar 

  • Mc Cormick CM (2010) An animal model of social instability stress in adolescence and risk for drugs of abuse. Physiol Behav 99:194–203

    Article  CAS  Google Scholar 

  • Mc Cormick CM, Ibrahim FN (2007) Locomotor activity to nicotine and Fos immunoreactivity in the paraventricular nucleus of the hypothalamus in adolescent socially-stressed rats. Pharmacol Biochem Behav 86:92–102

    Article  CAS  Google Scholar 

  • Mc Cormick CM, Mathews IZ (2007) HPA function in adolescence: role of sex hormones in its regulation and the enduring consequences of exposure to stressors. Pharmacol Biochem Behav 86:220–233

    Article  CAS  Google Scholar 

  • Mc Cormick CM, Mathews IZ (2010) Adolescent development, hypothalamic-pituitary-adrenal function, and programming of adult learning and memory. Prog Neuropsychopharmacol Biol Psychiatry 34:756–765

    Article  CAS  Google Scholar 

  • Mc Cormick CM, Mongillo DL, Simone JJ (2013) Age and adolescent social stress effects on fear extinction in female rats. Stress 16:678–688

    Article  CAS  Google Scholar 

  • Mc Cormick CM, Nixon F, Thomas C, Lowie B, Dyck J (2010) Hippocampal cell proliferation and spatial memory performance after social instability stress in adolescence in female rats. Behav Brain Res 208:23–29

    Article  Google Scholar 

  • Mc Cormick CM, Robarts D, Gleason E, Kelsey JE (2004) Stress during adolescence enhances locomotor sensitization to nicotine in adulthood in female, but not male, rats. Horm Behav 46:458–466

    Article  CAS  Google Scholar 

  • Mc Cormick CM, Smith C, Mathews IZ (2008) Effects of chronic social stress in adolescence on anxiety and neuroendocrine response to mild stress in male and female rats. Behav Brain Res 187:228–238

    Article  CAS  Google Scholar 

  • Mc Cormick CM, Thomas CM, Sheridan CS, Nixon F, Flynn JA, Mathews IZ (2012) Social instability stress in adolescent male rats alters hippocampal neurogenesis and produces deficits in spatial location memory in adulthood. Hippocampus 22:1300–1312

    Article  Google Scholar 

  • Mckinney WT (1989) Basis of development of animal models in psychiatry: an overview. In: Koob GF, Ehlers CL, Kupfer DJ (eds) Animal Models of Depression. Boston, Birkhäuser Boston

    Google Scholar 

  • Meaney MJ (2001) Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu Rev Neurosci 24:1161–1192

    Article  CAS  PubMed  Google Scholar 

  • Meng Q, Li N, Han X, Shao F, Wang W (2010) Peri-adolescence isolation rearing alters social behavior and nociception in rats. Neurosci Lett 480:25–29

    Article  CAS  PubMed  Google Scholar 

  • Miczek KA, Yap JJ, Covington HE, 3RD (2008) Social stress, therapeutics and drug abuse: preclinical models of escalated and depressed intake. Pharmacol Ther 120:102–128

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Momeni S, Segerstrom L, Roman E (2015) Supplier-dependent differences in intermittent voluntary alcohol intake and response to naltrexone in Wistar rats. Front Neurosci 9:424

    Article  PubMed  PubMed Central  Google Scholar 

  • Montagud-Romero S, Aguilar MA, Maldonado C, Manzanedo C, Minarro J, Rodriguez-Arias M (2015) Acute social defeat stress increases the conditioned rewarding effects of cocaine in adult but not in adolescent mice. Pharmacol Biochem Behav 135:1–12

    Article  CAS  PubMed  Google Scholar 

  • Moore NL, Gauchan S, Genovese RF (2012) Differential severity of anxiogenic effects resulting from a brief swim or underwater trauma in adolescent male rats. Pharmacol Biochem Behav 102:264–268

    Article  CAS  PubMed  Google Scholar 

  • Moore NL, Gauchan S, Genovese RF (2014) Adolescent traumatic stress experience results in less robust conditioned fear and post-extinction fear cue responses in adult rats. Pharmacol Biochem Behav 120:17–24

    Article  CAS  PubMed  Google Scholar 

  • Moriya Y, Kasahara Y, Hall FS, Sakakibara Y, Uhl GR, Tomita H, Sora I (2015) Sex differences in the effects of adolescent social deprivation on alcohol consumption in mu-opioid receptor knockout mice. Psychopharmacology (Berl) 232:1471–1482

    Article  CAS  Google Scholar 

  • Morrissey MD, Mathews IZ, Mc Cormick CM (2011) Enduring deficits in contextual and auditory fear conditioning after adolescent, not adult, social instability stress in male rats. Neurobiol Learn Mem 95:46–56

    Article  PubMed  Google Scholar 

  • National Institute of Child Health and Human Development 2006. The Health Behaviors In School-age Children (HBSC) 2005/2006 Survey. Division of Epidemiology Statistics & Prevention Research Eunice Kennedy Shriver National Institute of Child Health and Human Development/NIH/DHHS.

  • Negron-Oyarzo I, Perez MA, Terreros G, Munoz P, Dagnino-Subiabre A (2014) Effects of chronic stress in adolescence on learned fear, anxiety, and synaptic transmission in the rat prelimbic cortex. Behav Brain Res 259:342–353

    Article  PubMed  Google Scholar 

  • Nestler EJ, Hyman SE (2010) Animal models of neuropsychiatric disorders. Nat Neurosci 13:1161–1169

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nishio H, Tokumo K, Hirai T (2006) Effects of perinatal stress on the anxiety-related behavior of the adolescence mouse. Int J Dev Neurosci 24:263–268

    Article  CAS  PubMed  Google Scholar 

  • Noori HR, Helinski S, Spanagel R (2014) Cluster and meta-analyses on factors influencing stress-induced alcohol drinking and relapse in rodents. Addict Biol 19:225–232

    Article  CAS  PubMed  Google Scholar 

  • Novick AM, Mears M, Forster GL, Lei Y, Tejani-Butt SM, Watt MJ (2016) Adolescent social defeat alters N-methyl-D-aspartic acid receptor expression and impairs fear learning in adulthood. Behav Brain Res 304:51–59

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Novick AM, Miiller LC, Forster GL, WATT MJ (2013) Adolescent social defeat decreases spatial working memory performance in adulthood. Behav Brain Funct 9:39

    Article  PubMed  PubMed Central  Google Scholar 

  • Nylander I, Roman E (2013) Is the rodent maternal separation model a valid and effective model for studies on the early-life impact on ethanol consumption? Psychopharmacology (Berl) 229:555–569

    Article  CAS  Google Scholar 

  • O’Connor RM, Moloney RD, Glennon J, Vlachou S, Cryan JF (2015) Enhancing glutamatergic transmission during adolescence reverses early-life stress-induced deficits in the rewarding effects of cocaine in rats. Neuropharmacology 99:168–176

    Article  PubMed  CAS  Google Scholar 

  • Ota Y, Ago Y, Tanaka T, Hasebe S, Toratani Y, Onaka Y, Hashimoto H, Takuma K, Matsuda T (2015) Anxiolytic-like effects of restraint during the dark cycle in adolescent mice. Behav Brain Res 284:103–111

    Article  CAS  PubMed  Google Scholar 

  • Palm S, Hävermark Å, Meyerson BJ, Nylander I, ROMAN E (2011a) When is a Wistar a Wistar? Behavioral profiling of outbred Wistar rats from five different suppliers using the MCSF test. Appl Animal Behav Sci 135:128–137

    Article  Google Scholar 

  • Palm S, Roman E, Nylander I (2011b) Differences in voluntary ethanol consumption in Wistar rats from five different suppliers. Alcohol 45:607–614

    Article  PubMed  Google Scholar 

  • Palm S, Roman E, Nylander I (2012) Differences in basal and ethanol-induced levels of opioid peptides in Wistar rats from five different suppliers. Peptides 36:1–8

    Article  CAS  PubMed  Google Scholar 

  • Paus T (2005) Mapping brain maturation and cognitive development during adolescence. Trends Cogn Sci 9:60–68

    Article  PubMed  Google Scholar 

  • Peleg-Raibstein D, Feldon J (2011) Differential effects of post-weaning juvenile stress on the behaviour of C57BL/6 mice in adolescence and adulthood. Psychopharmacology (Berl) 214:339–351

    Article  CAS  Google Scholar 

  • Penasco S, Mela V, Lopez-Moreno JA, Viveros MP, Marco EM (2015) Early maternal deprivation enhances voluntary alcohol intake induced by exposure to stressful events later in life. Neural Plast 2015:342761

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Plotsky PM, Meaney MJ (1993) Early, postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats. Molecular Brain Research 18:195–200

    Article  CAS  PubMed  Google Scholar 

  • Pohl J, Olmstead MC, Wynne-Edwards KE, Harkness K, Menard JL (2007) Repeated exposure to stress across the childhood-adolescent period alters rats’ anxiety- and depression-like behaviors in adulthood: The importance of stressor type and gender. Behav Neurosci 121:462–474

    Article  PubMed  Google Scholar 

  • Post RJ, Dahlborg KM, O’Loughlin LE, Bloom CM (2014) Effects of juvenile exposure to predator odor on adolescent and adult anxiety and pain nociception. Physiol Behav 131:57–61

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pritchard LM, Hensleigh E, Lynch S (2012) Altered locomotor and stereotyped responses to acute methamphetamine in adolescent, maternally separated rats. Psychopharmacology (Berl) 223:27–35

    Article  CAS  Google Scholar 

  • Pryce CR, Feldon J (2003) Long-term neurobehavioural impact of the postnatal environment in rats: manipulations, effects and mediating mechanisms. Neurosci Biobehav Rev 27:57–71

    Article  PubMed  Google Scholar 

  • Raftogianni A, Diamantopoulou A, Alikaridis F, Stamatakis A, Stylianopoulou F (2012) Effects of interaction of an early experience of reward through maternal contact or its denial with social stress during adolescence on the serotonergic system and the stress responsiveness of adult female rats. Neuroscience 209:84–96

    Article  CAS  PubMed  Google Scholar 

  • Reich CG, Iskander AN, Weiss MS (2013) Cannabinoid modulation of chronic mild stress-induced selective enhancement of trace fear conditioning in adolescent rats. J Psychopharmacol 27:947–955

    Article  CAS  PubMed  Google Scholar 

  • Richter SH, Kastner N, Loddenkemper DH, Kaiser S, Sachser N (2016) A time to wean? Impact of weaning age on anxiety-like behaviour and stability of behavioural traits in full adulthood. PLoS One 11:e0167652

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rincon-Cortes M, Sullivan RM (2014) Early life trauma and attachment: immediate and enduring effects on neurobehavioral and stress axis development. Front Endocrinol (Lausanne) 5:33

    Google Scholar 

  • Rodriguez-Arias M, Navarrete F, Blanco-Gandia MC, Arenas MC, Bartoll-Andrés A, Aguilar MA, Rubio G, Miñarro J, Manzanares J (2016) Social defeat in adolescent mice increases vulnerability to alcohol consumption. Addiction Biology 21:87–97

    Article  CAS  PubMed  Google Scholar 

  • Roman E, Gustafsson L, Hyytia P, Nylander I (2005) Short and prolonged periods of maternal separation and voluntary ethanol intake in male and female ethanol-preferring AA and ethanol-avoiding ANA rats. Alcohol Clin Exp Res 29:591–601

    Article  PubMed  Google Scholar 

  • Romeo RD (2010) Adolescence: a central event in shaping stress reactivity. Dev Psychobiol 52:244–253

    PubMed  Google Scholar 

  • Romeo RD, Karatsoreos IN, Mc Ewen BS (2006) Pubertal maturation and time of day differentially affect behavioral and neuroendocrine responses following an acute stressor. Horm Behav 50:463–468

    Article  CAS  PubMed  Google Scholar 

  • Romeo RD, Mc Ewen BS (2006) Stress and the adolescent brain. Ann N Y Acad Sci 1094:202–214

    Article  CAS  PubMed  Google Scholar 

  • Safranski TJ, Lamberson WR, Keisler DH (1993) Correlations among three measures of puberty in mice and relationships with estradiol concentration and ovulation. Biol Reprod 48:669–673

    Article  CAS  PubMed  Google Scholar 

  • Sarro EC, Sullivan RM, Barr G (2014) Unpredictable neonatal stress enhances adult anxiety and alters amygdala gene expression related to serotonin and GABA. Neuroscience 258:147–161

    Article  CAS  PubMed  Google Scholar 

  • Saul ML, Tylee D, Becoats KT, Guerrero BG, Sweeney P, Helmreich DL, Fudge JL (2012) Long-term behavioral consequences of stress exposure in adolescent versus young adult rats. Behav Brain Res 229:226–234

    Article  PubMed  Google Scholar 

  • Schalinski I, Teicher MH, Nischk D, Hinderer E, Muller O, Rockstroh B (2016) Type and timing of adverse childhood experiences differentially affect severity of PTSD, dissociative and depressive symptoms in adult inpatients. BMC Psychiatry 16:295

    Article  PubMed  PubMed Central  Google Scholar 

  • Schmidt MV, Czisch M, Sterlemann V, Reinel C, Samann P, Muller MB (2009) Chronic social stress during adolescence in mice alters fat distribution in late life: prevention by antidepressant treatment. Stress 12:89–94

    Article  CAS  PubMed  Google Scholar 

  • Schneider P, Hannusch C, Schmahl C, Bohus M, Spanagel R, Schneider M (2014) Adolescent peer-rejection persistently alters pain perception and CB1 receptor expression in female rats. Eur Neuropsychopharmacol 24:290–301

    Article  CAS  PubMed  Google Scholar 

  • Serra M, Pisu MG, Floris I, Biggio G (2005) Social isolation-induced changes in the hypothalamic-pituitary-adrenal axis in the rat. Stress 8:259–264

    Article  CAS  PubMed  Google Scholar 

  • Shetgiri R (2013) Bullying and Victimization Among Children. Advances in pediatrics 60:33–51

    Article  PubMed  PubMed Central  Google Scholar 

  • Shin SY, Han SH, Woo RS, Jang SH, Min SS (2016) Adolescent mice show anxiety- and aggressive-like behavior and the reduction of long-term potentiation in mossy fiber-CA3 synapses after neonatal maternal separation. Neuroscience 316:221–231

    Article  CAS  PubMed  Google Scholar 

  • Shriner AM, Drever FR, Metz GA (2009) The development of skilled walking in the rat. Behav Brain Res 205:426–435

    Article  PubMed  PubMed Central  Google Scholar 

  • Siviy SM, Crawford CA, Akopian G, Walsh JP (2011) Dysfunctional play and dopamine physiology in the Fischer 344 rat. Behav Brain Res 220:294–304

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Skelly MJ, Chappell AE, Carter E, Weiner JL (2015) Adolescent social isolation increases anxiety-like behavior and ethanol intake and impairs fear extinction in adulthood: possible role of disrupted noradrenergic signaling. Neuropharmacology 97:149–159

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Snyder K, Barry M, Plona Z, Ho A, Zhang XY, Valentino RJ (2015a) The impact of social stress during adolescence or adulthood and coping strategy on cognitive function of female rats. Behav Brain Res 286:175–183

    Article  PubMed  PubMed Central  Google Scholar 

  • Snyder KP, Barry M, Valentino RJ (2015b) Cognitive impact of social stress and coping strategy throughout development. Psychopharmacology (Berl) 232:185–195

    Article  CAS  Google Scholar 

  • Song M, Wang XY, Zhao M, Wang XY, Zhai HF, Lu L (2007) Role of stress in acquisition of alcohol-conditioned place preference in adolescent and adult mice. Alcohol Clin Exp Res 31:2001–2005

    Article  PubMed  Google Scholar 

  • Spivey J, Barrett D, Padilla E, Gonzalez-Lima F (2008) Mother-infant separation leads to hypoactive behavior in adolescent Holtzman rats. Behav Processes 79:59–65

    Article  PubMed  PubMed Central  Google Scholar 

  • Spivey JM, Shumake J, Colorado RA, Conejo-Jimenez N, Gonzalez-Pardo H, Gonzalez-Lima F (2009) Adolescent female rats are more resistant than males to the effects of early stress on prefrontal cortex and impulsive behavior. Dev Psychobiol 51:277–288

    Article  PubMed  PubMed Central  Google Scholar 

  • Sterlemann V, Rammes G, Wolf M, Liebl C, Ganea K, Muller MB, Schmidt MV (2010) Chronic social stress during adolescence induces cognitive impairment in aged mice. Hippocampus 20:540–549

    PubMed  Google Scholar 

  • Suo L, Zhao L, Si J, Liu J, Zhu W, Chai B, Zhang Y, Feng J, Ding Z, Luo Y, Shi H, Shi J, Lu L (2013) Predictable chronic mild stress in adolescence increases resilience in adulthood. Neuropsychopharmacology 38:1387–1400

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taylor SB, Taylor AR, Koenig JI (2013) The interaction of disrupted type II neuregulin 1 and chronic adolescent stress on adult anxiety- and fear-related behaviors. Neuroscience 249:31–42

    Article  CAS  PubMed  Google Scholar 

  • Teicher MH, Andersen SL, Polcari A, Anderson CM, Navalta CP, Kim DM (2003) The neurobiological consequences of early stress and childhood maltreatment. Neurosci Biobehav Rev 27:33–44

    Article  PubMed  Google Scholar 

  • Tokumo K, Hirai T, Nishino H (2006) Effects of perinatal stress on the emotion-related behavior of the adolescent mouse. Biol Pharm Bull 29:1036–1038

    Article  CAS  PubMed  Google Scholar 

  • Toledo-Rodriguez M, Sandi C (2007) Stress before puberty exerts a sex- and age-related impact on auditory and contextual fear conditioning in the rat. Neural Plast 2007:71203

    Article  PubMed  PubMed Central  Google Scholar 

  • Tomkins SS (1966) Psychological model for smoking behavior. Am J Public Health Nations Health 56(12 Suppl):17–20

    Article  PubMed Central  Google Scholar 

  • Tornatzky W, Miczek KA (1993) Long-term impairment of autonomic circadian rhythms after brief intermittent social stress. Physiol Behav 53:983–993

    Article  CAS  PubMed  Google Scholar 

  • Tsoory M, Richter-Levin G (2006) Learning under stress in the adult rat is differentially affected by 'juvenile' or 'adolescent' stress. Int J Neuropsychopharmacol 9:713–728

    Article  PubMed  Google Scholar 

  • Uysal N, Sisman AR, Dayi A, Ozbal S, Cetin F, Baykara B, Aksu I, Tas A, Cavus SA, Gonenc-Arda S, Buyuk E (2012) Acute footshock-stress increases spatial learning-memory and correlates to increased hippocampal BDNF and VEGF and cell numbers in adolescent male and female rats. Neurosci Lett 514:141–146

    Article  CAS  PubMed  Google Scholar 

  • van Waes V, Darnaudery M, Marrocco J, Gruber SH, Talavera E, Mairesse J, van Camp G, Casolla B, Nicoletti F, Mathe AA, Maccari S, Morley-Fletcher S (2011) Impact of early life stress on alcohol consumption and on the short- and long-term responses to alcohol in adolescent female rats. Behav Brain Res 221:43–49

    Article  PubMed  CAS  Google Scholar 

  • Varlinskaya EI, Doremus-Fitzwater TL, Spear LP (2010) Repeated restraint stress alters sensitivity to the social consequences of ethanol in adolescent and adult rats. Pharmacol Biochem Behav 96:228–235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Varlinskaya EI, Spear LP (2012) Increases in anxiety-like behavior induced by acute stress are reversed by ethanol in adolescent but not adult rats. Pharmacol Biochem Behav 100:440–450

    Article  CAS  PubMed  Google Scholar 

  • Varlinskaya EI, Spear LP (2015) Social consequences of ethanol: impact of age, stress, and prior history of ethanol exposure. Physiol Behav 148:145–150

    Article  CAS  PubMed  Google Scholar 

  • Varlinskaya EI, Truxell EM, Spear LP (2013) Repeated restraint stress alters sensitivity to the social consequences of ethanol differentially in early and late adolescent rats. Pharmacol Biochem Behav 113:38–45

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vazquez DM, Akil H (1993) Pituitary-adrenal response to ether vapor in the weanling animal: characterization of the inhibitory effect of glucocorticoids on adrenocorticotropin secretion. Pediatr Res 34:646–653

    Article  CAS  PubMed  Google Scholar 

  • ver Hoeve ES, Kelly G, Luz S, Ghanshani S, Bhatnagar S (2013) Short-term and long-term effects of repeated social defeat during adolescence or adulthood in female rats. Neuroscience 249:63–73

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vidal J, Bie J, Granneman RA, Wallinga AE, Koolhaas JM, Buwalda B (2007) Social stress during adolescence in Wistar rats induces social anxiety in adulthood without affecting brain monoaminergic content and activity. Physiol Behav 92:824–830

    Article  CAS  PubMed  Google Scholar 

  • Vidal J, Buwalda B, Koolhaas JM (2011a) Differential long-term effects of social stress during adolescence on anxiety in Wistar and wild-type rats. Behav Processes 87:176–182

    Article  PubMed  Google Scholar 

  • Vidal J, Buwalda B, Koolhaas JM (2011b) Male Wistar rats are more susceptible to lasting social anxiety than Wild-type Groningen rats following social defeat stress during adolescence. Behav Processes 88:76–80

    Article  PubMed  Google Scholar 

  • Wang J, Iannotti RJ, Nansel TR (2009) School bullying among adolescents in the United States: physical, verbal, relational, and cyber. J Adolesc Health 45:368–375

    Article  PubMed  PubMed Central  Google Scholar 

  • Warren BL, Sial OK, Alcantara LF, Greenwood MA, Brewer JS, Rozofsky JP, Parise EM, Bolanos-Guzman CA (2014) Altered gene expression and spine density in nucleus accumbens of adolescent and adult male mice exposed to emotional and physical stress. Dev Neurosci 36:250–260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Watt MJ, Burke AR, Renner KJ, Forster GL (2009) Adolescent male rats exposed to social defeat exhibit altered anxiety behavior and limbic monoamines as adults. Behav Neurosci 123:564–576

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weintraub A, Singaravelu J, Bhatnagar S (2010) Enduring and sex-specific effects of adolescent social isolation in rats on adult stress reactivity. Brain Res 1343:83–92

    Article  CAS  PubMed  Google Scholar 

  • Weiss IC, Domeney AM, Moreau JL, Russig H, Feldon J (2001) Dissociation between the effects of pre-weaning and/or post-weaning social isolation on prepulse inhibition and latent inhibition in adult Sprague-Dawley rats. Behav Brain Res 121:207–218

    Article  CAS  PubMed  Google Scholar 

  • Wilkin MM, Waters P, Mc Cormick CM, Menard JL (2012) Intermittent physical stress during early- and mid-adolescence differentially alters rats’ anxiety- and depression-like behaviors in adulthood. Behav Neurosci 126:344–360

    Article  PubMed  Google Scholar 

  • Willey AR, Spear LP (2013) Effects of acute ethanol administration and chronic stress exposure on social investigation and 50kHz ultrasonic vocalizations in adolescent and adult male Sprague-Dawley rats. Pharmacol Biochem Behav 105:17–25

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Willner P (1997) Validity, reliability and utility of the chronic mild stress model of depression: a 10-year review and evaluation. Psychopharmacology (Berl) 134:319–329

    Article  CAS  Google Scholar 

  • Wills TA, Knapp DJ, Overstreet DH, Breese GR (2010) Interactions of stress and CRF in ethanol-withdrawal induced anxiety in adolescent and adult rats. Alcohol Clin Exp Res 34:1603–1612

  • Wills TA, Vaughan RJ (1989) Social support and substance use in early adolescence. Behav Med 12(4):321–339. https://doi.org/10.1007/BF00844927

  • Wood SK (2014) Individual differences in the neurobiology of social stress: implications for depression-cardiovascular disease comorbidity. Curr Neuropharmacol 12:205–211

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wright KM, Dileo A, MCDANNALD MA (2015) Early adversity disrupts the adult use of aversive prediction errors to reduce fear in uncertainty. Front Behav Neurosci 9:227

  • Wright LD, Hebert KE, Perrot-Sinal TS (2008) Periadolescent stress exposure exerts long-term effects on adult stress responding and expression of prefrontal dopamine receptors in male and female rats. Psychoneuroendocrinology 33:130–142

    Article  CAS  PubMed  Google Scholar 

  • Wright LD, Muir KE, Perrot TS (2012) Enhanced stress responses in adolescent versus adult rats exposed to cues of predation threat, and peer interaction as a predictor of adult defensiveness. Dev Psychobiol 54:47–69

    Article  CAS  PubMed  Google Scholar 

  • Wright LD, Muir KE, Perrot TS (2013) Stress responses of adolescent male and female rats exposed repeatedly to cat odor stimuli, and long-term enhancement of adult defensive behaviors. Dev Psychobiol 55:551–567

    Article  CAS  PubMed  Google Scholar 

  • Wulsin AC, Wick-Carlson D, Packard BA, Morano R, Herman JP (2016) Adolescent chronic stress causes hypothalamo-pituitary-adrenocortical hypo-responsiveness and depression-like behavior in adult female rats. Psychoneuroendocrinology 65:109–117

    Article  CAS  PubMed  Google Scholar 

  • Yee N, Schwarting RK, Fuchs E, WOHR M (2012) Juvenile stress potentiates aversive 22-kHz ultrasonic vocalizations and freezing during auditory fear conditioning in adult male rats. Stress 15:533–544

    Article  PubMed  Google Scholar 

  • Younes-Rapozo V, Moura EG, Manhaes AC, Peixoto-Silva N, de Oliveira E, Lisboa PC (2015) Early weaning by maternal prolactin inhibition leads to higher neuropeptide Y and astrogliosis in the hypothalamus of the adult rat offspring. Br J Nutr 113:536–545

    Article  CAS  PubMed  Google Scholar 

  • Zaidan H, Gaisler-Salomon I (2015) Prereproductive stress in adolescent female rats affects behavior and corticosterone levels in second-generation offspring. Psychoneuroendocrinology 58:120–129

    Article  CAS  PubMed  Google Scholar 

  • Zalsman G, Gutman A, Shbiro L, Rosenan R, Mann JJ, Weller A (2015) Genetic vulnerability, timing of short-term stress and mood regulation: a rodent diffusion tensor imaging study. Eur Neuropsychopharmacol 25:2075–2085

    Article  CAS  PubMed  Google Scholar 

  • Zamberletti E, Prini P, Speziali S, Gabaglio M, Solinas M, Parolaro D, Rubino T (2012) Gender-dependent behavioral and biochemical effects of adolescent delta-9-tetrahydrocannabinol in adult maternally deprived rats. Neuroscience 204:245–257

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Abdallah CG, Chen Y, Huang T, Huang Q, Xu C, Xiao Y, Liu Y, Ding Y, Wu R (2013) Behavioral deficits, abnormal corticosterone, and reduced prefrontal metabolites of adolescent rats subject to early life stress. Neurosci Lett 545:132–137

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang W, Rosenkranz JA (2013) Repeated restraint stress enhances cue-elicited conditioned freezing and impairs acquisition of extinction in an age-dependent manner. Behav Brain Res 248:12–24

    Article  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Department of Psychology, Tufts University, 530 Boston Avenue, Medford, MA, 02155, USA

    Kate McDonnell-Dowling & Klaus A. Miczek

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  1. Kate McDonnell-Dowling
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  2. Klaus A. Miczek
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Correspondence to Kate McDonnell-Dowling.

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McDonnell-Dowling, K., Miczek, K.A. Alcohol, psychomotor-stimulants and behaviour: methodological considerations in preclinical models of early-life stress. Psychopharmacology 235, 909–933 (2018). https://doi.org/10.1007/s00213-018-4852-5

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  • DOI: https://doi.org/10.1007/s00213-018-4852-5

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