5,954
Views
150
CrossRef citations to date
0
Altmetric
Translational Research

Behavioral methods to study anxiety in rodents

Métodos conductuales para estudiar la ansiedad en roedores

Méthodes comportementales d'étude de l'anxiété chez les rongeurs

, &

REFERENCES

  • HymanS.Mental health: depression needs large human-genetics studies.Nature.2014515752618919125391945
  • CuthbertBN.InselTR.Toward the future of psychiatric diagnosis: the seven pillars of RDoCBMC Med.20131112623672542
  • WalkerDL.ToufexisDJ.DavisM.Role of the bed nucleus of the stria terminalis versus the amygdala in fear, stress, and anxiety.Eur J Pharmacol.20034631-319921612600711
  • DavisM.WalkerDL.MilesL.GrillonC.Phasic vs sustained fear in rats and humans: role of the extended amygdala in fear vs anxiety.Neuropsychopharmacology.201035110513519693004
  • WalkerDL.DavisM.Role of the extended amygdala in short-duration versus sustained fear: a tribute to Dr. Lennart Heimer.Brain Struct Funct.20082131-2294218528706
  • DavisM.Are different parts of the extended amygdala involved in fear versus anxiety?Biol Psychiatry.19984412123912479861467
  • WalkerDL.DavisM.Role of the extended amygdala in short-duration versus sustained fear: a tribute to Dr. Lennart Heimer.Brain Struct Funct.20082131-2294218528706
  • WalkerDL.MilesLA.DavisM.Selective participation of the bed nucleus of the stria terminalis and CRF in sustained anxiety-like versus phasic fear-like responses.Prog Neuropsychopharmacol Biol Psychiatry.20093381291130819595731
  • BourinM.Animal models for screening anxiolytic-like drugs: a perspective.Dialogues Clin Neurosci.201517329530326487810
  • CrawleyJN.Neuropharmacology specificity of a simple animal model for the behavioral actions of benzodiazepines.Pharmacol Biochem Behav.19811556956996118883
  • CrawleyJ.GoodwinFK.Preliminary report of a simple animal behavior model for the anxiolytic effects of benzodiazepines.Pharmacol Biochem Behav.1980132167170
  • BourinM.HascoetM.The mouse light/dark box test.Eur J Pharmacol.20034631-3556512600702
  • HandleySL.MithaniS.Effects of alpha-adrenoceptor agonists and antagonists in a maze-exploration model of 'fear'-motivated behaviour.Naunyn Schmiedebergs Arch Pharmacol.19843271156149466
  • PellowS.FileSE.Anxiolytic and anxiogenic drug effects on exploratory activity in an elevated plus-maze: a novel test of anxiety in the rat.Pharmacol Biochem Behav.19862435255292871560
  • FileSE.HydeJR.Can social interaction be used to measure anxiety?Br J Pharmacol.19786211924563752
  • FileSE.SethP.A review of 25 years of the social interaction test.Eur J Pharmacol.20034631-3355312600701
  • FileSE.Animal models for predicting clinical efficacy of anxiolytic drugs: social behaviour.Neuropsychobiology1985131-255622863779
  • DeaconRM.Hyponeophagia: a measure of anxiety in the mouse.J Vis Exp.2011 51doi:10.37912613
  • DulawaSC.HenR.Recent advances in animal models of chronic antidepressant effects: the novelty-induced hypophagia test.Neurosci Biobehav Rev.2005294-577178315890403
  • BourinM.Petit-DemouliereB.DhonnchadhaBN.HascoetM.Animal models of anxiety in mice.Fundam Clin Pharmacol.200721656757418034657
  • DielenbergRA.McGregorIS.Defensive behavior in rats towards predatory odors: a review.Neurosci Biobehav Rev.2001257-859760911801285
  • BlanchardRJ.BlanchardDC.Attack and defense in rodents as etho-experimental models for the study of emotion.Prog Neuropsychopharmacol Biol Psychiatry.198913supplS3S142694228
  • ZangrossiH.Jr FileSE.Behavioral consequences in animal tests of anxiety and exploration of exposure to cat odor.Brain Res Bull.199229343813881393611
  • CattarelliM.ChanelJ.Influence of some biologically meaningful odorants on the vigilance states of the rat.Physiol Behav1979235831838523535
  • WaddellJ.MorrisRW.BoutonME.Effects of bed nucleus of the stria terminalis lesions on conditioned anxiety: aversive conditioning with long-duration conditional stimuli and reinstatement of extinguished fear.Behav Neurosci.2006120232433616719697
  • DavisM.WalkerDL.LeeY.Roles of the amygdala and bed nucleus of the stria terminalis in fear and anxiety measured with the acoustic startle reflex. Possible relevance to PTSD.Ann N Y Acad Sci.19978213053319238214
  • FanselowMS.Neural organization of the defensive behavior system responsible for fear.Psychon Bull Rev.19941442943824203551
  • WillnerP.Validity, reliability and utility of the chronic mild stress model of depression: a 10-year review and evaluation.Psychopharmacology (Berl).19971344319329
  • WillnerP.The chronic mild sterss (CMS) model of depression: history, evaluation and usage.Neurobiol Stress.2017 6789328229111
  • HammackSE.CheungJ.RhodesKM.et alChronic stress increases pituitary adenylate cyclase-activating peptide (PACAP) and brain-derived neurotrophic factor (BDNF) mRNA expression in the bed nucleus of the stria terminalis (BNST): roles for PACAP in anxiety-like behavior.Psychoneuroendocrinology.200934683384319181454
  • WillnerP.Chronic mild stress (CMS) revisited: consistency and behavioural-neurobiological concordance in the effects of CMS.Neuropsychobiology.20055229011016037678
  • YamamotoS.MorinobuS.TakeiS.et alSingle prolonged stress: toward an animal model of posttraumatic stress disorder.Depress Anxiety.200926121110111719918929
  • LiberzonI.KrstovM.YoungEA.Stress-restress: effects on ACTH and fast feedback.Psychoneuroendocrinology.19972264434539364622
  • TakahashiT.MorinobuS.IwamotoY.YamawakiS.Effect of paroxetine on enhanced contextual fear induced by single prolonged stress in rats.Psychopharmacology (Berl).2006189216517317031709
  • YamamotoS.MorinobuS.FuchikamiM.KurataA.KozuruT.YamawakiS.Effects of single prolonged stress and D-cycloserine on contextual fear extinction and hippocampal NMDA receptor expression in a rat model of PTSD.Neuropsychopharmacology.20083392108211617957211
  • MiczekKA.YapJJ.CovingtonHE, 3rd.Social stress, therapeutics and drug abuse: preclinical models of escalated and depressed intake.Pharmacol Ther2008120210212818789966
  • BertonO.McClungCA.DileoneRJ.et alEssential role of BDNF in the mesolimbic dopamine pathway in social defeat stress.Science.2006311576286486816469931
  • GoldenSA.CovingtonHE, 3rd.BertonO.RussoSJ.A standardized protocol for repeated social defeat stress in mice.Nat Protoc.2011681183119121799487
  • IniguezSD.RiggsLM.NietoSJ.et alSocial defeat stress induces a depression-like phenotype in adolescent male c57BL/6 mice.Stress.201417324725524689732
  • KinseySG.BaileyMT.SheridanJF.PadgettDA.AvitsurR.Repeated social defeat causes increased anxiety-like behavior and alters splenocyte function in C57BL/6and CD-1 mice.Brain Behav Immun.200721445846617178210
  • DonahueRJ.MuschampJW.RussoSJ.NestlerEJ.CarlezonWA Jr.Effects of striatal ΔFosB overexpression and ketamine on social defeat stress-induced anhedonia in mice.Biol Psychiatry.201476755055824495460
  • LupienSJ.McEwenBS.GunnarMR.HeimC.Effects of stress throughout the lifespan on the brain, behaviour and cognition.Nat Rev Neurosci.200910643444519401723
  • NemeroffCB.Neurobiological consequences of childhood trauma.J Clin Psychiatry.200465suppl 11828
  • NishiM.Horii-HayashiN.SasagawaT.Effects of early life adverse experiences on the brain: implications from maternal separation models in rodents.Front Neurosci.2014816624987328
  • PryceCR.Ruedi-BettschenD.DettlingAC.FeldonJ.Early life stress: long-term physiological impact in rodents and primates.News Physiol Sci.20021715015512136043
  • van OersHJ.de KloetER.LevineS.Early vs. late maternal deprivation differentially alters the endocrine and hypothalamic responses to stress.Brain Res Dev Brain Res.199811122452529838147
  • MoletJ.MarasPM.Avishai-ElinerS.BaramTZ.Naturalistic rodent models of chronic early-life stress.Dev Psychobiol.20145681675168824910169
  • IvyAS.BrunsonKL.SandmanC.BaramTZ.Dysfunctional nurturing behavior in rat dams with limited access to nesting material: a clinically relevant model for early-life stress.Neuroscience.200815431132114218501521
  • BrunsonKL.KramarE.LinB.et alMechanisms of late-onset cognitive decline after early-life stress.J Neurosci.200525419328933816221841
  • Dalle MolleR.PortellaAK.GoldaniMZ.et alAssociations between parenting behavior and anxiety in a rodent model and a clinical sample: relationship to peripheral BDNF levels.Transl Psychiatry.20122e19523168995
  • HuizinkAC.de MedinaPG.MulderEJ.VisserGH.BuitelaarJK.Psychological measures of prenatal stress as predictors of infant temperament.J Am Acad Child Adolesc Psychiatry.20024191078108512218429
  • de WeerthC.van HeesY.BuitelaarJK.Prenatal maternal cortisol levels and infant behavior during the first 5 months.Early Hum Dev.200374213915114580753
  • WeinstockM.The long-term behavioural consequences of prenatal stress.Neurosci Biobehav Rev.20083261073108618423592
  • EstesML.McAllisterAK.Maternal immune activation: implications for neuropsychiatric disorders.Science.2016353630177277727540164
  • BabriS.DoostiMH.SalariAA.Strain-dependent effects of prenatal maternal immune activation on anxiety- and depression-like behaviors in offspring.Brain Behav Immun.20143716417624326014
  • GiovanoliS.EnglerH.EnglerA.et alStress in puberty unmasks latent neuropathological consequences of prenatal immune activation in mice.Science.201333961231095109923449593
  • HaskellSG.GordonKS.MattocksK.et alGender differences in rates of depression, PTSD, pain, obesity, and military sexual trauma among Connecticut War Veterans of Iraq and Afghanistan.J Womens Health (Larchmt).201019226727120109115
  • ResslerKJ.MercerKB.BradleyB.et alPost-traumatic stress disorder is associated with PACAP and the PAC1 receptor.Nature.2011470733549249721350482
  • RamikieTS.ResslerKJ.Stress-related disorders, pituitary adenylate cyclase-activating peptide (PACAP)ergic system, and sex differences.Dialogues Clin Neurosci.201618440341328179812
  • ShimamotoA.DeboldJF.HollyEN.MiczekKA.Blunted accumbal dopamine response to cocaine following chronic social stress in female rats: exploring a link between depression and drug abuse.Psychopharmacology (Berl).2011218127127921638221
  • TrainorBC.PrideMC.Villalon LanderosR.et alSex differences in social interaction behavior following social defeat stress in the monogamous California mouse (Peromyscus californicus).PLoS One.201162e1740521364768
  • GrueneTM.FlickK.StefanoA.SheaSD.ShanskyRM.Sexually divergent expression of active and passive conditioned fear responses in rats.Elife.20154 doi:07554eLife11352
  • BaleTL.EppersonCN.Sex as a biological variable: who, what, when, why, and how.Neuropsychopharmacology.201742238639627658485
  • DucottetC.BelzungC.Correlations between behaviours in the elevated plus-maze and sensitivity to unpredictable subchronic mild stress: evidence from inbred strains of mice.Behav Brain Res.2005156115316215474660
  • van BogaertMJ.GroeninkL.OostingRS.WestphalKG.van der GugtenJ.OlivierB.Mouse strain differences in autonomic responses to stress. Genes Brain Behav20065213914916507005
  • SanfordLD.YangL.WellmanLL.DongE.TangX.Mouse strain differences in the effects of corticotropin releasing hormone (CRH) on sleep and wakefulness.Brain Res.200811909410418053970
  • JenniferC.ChanAH.BaleTL.Strained in planning your mouse background? Using the HPA stress axis as a biological readout for backcrossing strategies.Neuropsychopharmacology.2017 Mar 31. Epub ahead of print. doi:10.1038/npp. 2017.66
  • AlexandrovV.BrunnerD.HananiaT.LeahyE.High-throughput analysis of behavior for drug discovery.Eur J Pharmacol.2015750828925592319
  • WiltschkoAB.JohnsonMJ.IurilliG.et alMapping sub-second structure in mouse behavior.Neuron.20158861121113526687221
  • FuzesiT.DaviuN.Wamsteeker CusulinJl.BoninRP.BainsJS.Hypothalamic CRH neurons orchestrate complex behaviours after stress.Nat Commun.201671193727306314
  • HammAO.RichterJ.Pane-FarreCA.When the threat comes from inside the body: a neuroscience based learning perspective of the etiology of panic disorder.Restor Neurol Neurosci.2014321799323803388
  • DavisM.AntoniadisEA.AmaralDG.WinslowJT.Acoustic startle reflex in rhesus monkeys: a review.Rev Neurosci.2008192-317118518751523
  • American Psychiatric Association.Diagnostic and Statistical Manual of Mental Disorders, 5th ed. Washington, DC: American Psychiatric Association.2013
  • GrillonC.Startle reactivity and anxiety disorders: aversive conditioning, context, and neurobiology.Biol Psychiatry2002521095897512437937
  • WalkerDL.DavisM.Light enhanced startle: futher pharmacological and behavioral characterization.Psychopharmacology.200215930431011862363
  • WalkerDL.DavisM.Double dissociation between the involvement of the bed nucleus of the stria terminalis and the central nucleus of the amygdala in startle increases produced by conditioned versus unconditioned fear.J Neurosci.19971723937593839364083
  • de JonghR.GroeninkL.van Der GugtenJ.OlivierB.The light-enhanced startle paradigm as a putative animal model for anxiety: effects of chlordiazepoxide, flesinoxan and fluvoxamine.Psychopharmacology (Berl).2002159217618011862346
  • GrillonC.AmeliR.Effects of threat of shock, shock electrode placement and darkness on startle.IntJ Psychophysiol.19982832232319545658
  • MuhlbergerA.WieserMJ.PauliP.Darkness-enhanced startle responses in ecologically valid environments: a virtual tunnel driving experiment.Biol Psychol.2008771475217950519
  • BockerKB.BaasJM.KenemansJL.VerbatenMN.Stimulus-preceding negativity induced by fear: a manifestation of affective anticipation.Int J Psychophysiol.2001431779011742686
  • MorganCA. 3rdSouthwickSM.GrillonC.DavisM.KrystalJH.CharneyDS.Yohimbine-facilitated acoustic startle reflex in humans.Psychopharmacology (Berl).199311033423467831429
  • HolmesAJ.PizzagalliDA.Spatiotemporal dynamics of error processing dysfunctions in major depressive disorder.Arch Gen Psychiatry.200865217918818250256
  • ElliottR.SahakianBJ.McKayAP.HerrodJJ.RobbinsTW.PaykelES.Neuropsychological impairments in unipolar depression: the influence of perceived failure on subsequent performance.Psychol Med.19962659759898878330
  • BeatsBC.SahakianBJ.LevyR.Cognitive performance in tests sensitive to frontal lobe dysfunction in the elderly depressed.Psychol Med.19962635916038733217
  • RobbinsTW.The 5-choice serial reaction time task: behavioural pharmacology and functional neurochemistry.Psychopharmacology (Berl).20021633-436238012373437
  • Van't VeerA.YanoJM.CarrollFI.CohenBM.CarlezonWA Jr.Corticotropin-releasing factor (CRF)-induced disruption of attention in rats is blocked by the kappa-opioid receptor antagonist JDTic.Neuropsychopharmacology.201237132809281622948977
  • DonahueRJ.VenkataramanA.CarrollFI.MeloniEG.CarlezonWA Jr.Pituitary adenylate cyclase-activating polypeptide disrupts motivation, social interaction, and attention in male sprague dawley rats.Biol Psychiatry.2016801295596426229039
  • PaineTA.TomasiewiczHC.ZhangK.CarlezonWA Jr.Sensitivity of the five-choice serial reaction time task to the effects of various psychotropic drugs in Sprague-Dawley rats.Biol Psychiatry.200762668769317343834
  • BeardC.DonahueRJ.DillonDG.et alAbnormal error processing in depressive states: a translational examination in humans and rats.Transl Psychiatry.20155e56425966364
  • BolandEM.RossRJ.Recent advances in the study of sleep in the anxiety disorders, obsessive-compulsive disorder, and posttraumatic stress disorder.Psychiatr Clin North Am.201538476177626600107
  • Pace-SchottEF.GermainA.Milad.MR.Sleep and REM sleep disturbance in the pathophysiology of PTSD: the role of extinction memory.Biol Mood Anxiety Disord.20155326034578
  • PalaginiL.BaglioniC.CiapparelliA.GemignaniA.RiemannD.REM sleep dysregulation in depression: state of the art.Sleep Med Rev.201317537739023391633
  • RampinC.CespuglioR.ChastretteN.JouvetM.Immobilisation stress induces a paradoxical sleep rebound in rat.Neurosci Lett.199112621131181922920
  • BonnetC.LegerL.BaubetV.DebillyG.CespuglioR.Influence of a 1 h immobilization stress on sleep states and corticotropin-like intermediate lobe peptide (CLIP or ACTH18-39, Ph-ACTH18-39) brain contents in the rat.Brain Res.1997751154639098568
  • MoreauJL.ScherschlichtR.JenckF.MartinJR.Chronic mild stressinduced anhedonia model of depression; sleep abnormalities and curative effects of electroshock treatment.Behav Pharmacol.19956768268711224370
  • CheetaS.RuigtG.van ProosdijJ.WillnerP.Changes in sleep architecture following chronic mild stress.Biol Psychiatry.19974144194279034536
  • Vazquez-PalaciosG.Velazquez-MoctezumaJ.Effect of electric foot shocks, immobilization, and corticosterone administration on the sleepwake pattern in the rat.Physiol Behav.2000711-2232811134681
  • PawlykAC.MorrisonAR.RossRJ.BrennanFX.Stress-induced changes in sleep in rodents: models and mechanisms.Neurosci Biobehav Rev.20083219911717764741
  • MangGM.FrankenP.Sleep and EEG phenotyping in mice.Curr Protoc Mouse Biol.201221557426069005
  • LundtA.WormuthC.SiwekME.et alEEG radiotelemetry in small laboratory rodents: a powerful state-of-the art approach in neuropsychiatry, neurodegenerative, and epilepsy research.Neural Plast.201620168213878