Abstract
Posttraumatic stress disorder (PTSD) is a trauma- and stressor-related disorder that is a source of significant societal and economic costs. Although it is not possible to fully model human psychiatric disorders using animal models, physiological responses to trauma and stressors, including hypothalamic-pituitary-adrenal (HPA) axis responses, autonomic nervous system responses, and immune responses, are highly conserved across mammalian species. Each of these physiological response systems, in turn, has been implicated in determining risk of development of PTSD symptoms, or contributing to PTSD severity, in humans, suggesting that understanding mechanisms underlying these responses may lead to novel therapeutic strategies for the prevention or treatment of PTSD. Furthermore, individual variability in physiological responses to trauma and stressors is thought to be an important determinant of stress vulnerability or stress resilience; therefore, understanding mechanisms underlying individual variability in physiological responses to trauma or stressor exposure has promise to increase our understanding of mechanisms underlying vulnerability to development of PTSD and persistence of PTSD symptoms. Here we describe a model of inescapable stress exposure in rats that has contributed to our understanding of the mechanisms underlying stress vulnerability and stress resilience. Given that PTSD is more common in females than males, we also highlight the need for increased focus on inclusion of both males in females in future studies.
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References
Sareen J (2018) Posttraumatic stress disorder in adults: epidemiology, pathophysiology, clinical manifestations, course, assessment, and diagnosis. Up to date [online]. Version May 2023
Sandars NK (1972) The epic of Gilgamesh. Penguin, London
Ben-Ezra M (2004) Trauma in antiquity: 4000 year old post-traumatic reactions? Stress Health 20:121–125
Geppert C (2021) An anniversary postponed and a diagnosis delayed: Vietnam and PTSD. Fed Pract 38:200–201
American Psychiatric Association (2013) Diagnostic and Statistical Manual of Mental Disorders: (5th ed). Arlington, VA
Ross RJ, Ball WA, Sullivan KA et al (1989) Sleep disturbance as the hallmark of posttraumatic stress disorder. Am J Psychiatry 146(6):697–707
Inman DJ, Silver SM, Doghramji K (1990) Sleep disturbance in post-traumatic stress disorder: a comparison with non-PTSD insomnia. J Trauma Stress 3:429–437
Lamarche LJ, De Koninck J (2007) Sleep disturbance in adults with posttraumatic stress disorder: a review. J Clin Psychiatry 68(8):1257–1270
Pace-Schott EF, Germain A, Milad MR (2015) Sleep and REM sleep disturbance in the pathophysiology of PTSD: the role of extinction memory. Biol Mood Anxiety Disord 5:1–19
Otis JD, Keane TM, Kerns RD (2003) An examination of the relationship between chronic pain and post-traumatic stress disorder. J Rehabil Res Dev 40:397–406
Scioli-Salter ER, Forman DE, Otis JD et al (2015) The shared neuroanatomy and neurobiology of comorbid chronic pain and PTSD: therapeutic implications. Clin J Pain 31:363–374
Sharp TJ, Harvey AG (2001) Chronic pain and posttraumatic stress disorder: mutual maintenance? Clin Psychol Rev 21:857–877
Asmundson GJ, Hadjistavropolous HD (2006) Addressing shared vulnerability for comorbid PTSD and chronic pain: a cognitive-behavioral perspective. Cogn Behav Pract 13:8–16
Shipherd JC, Keyes M, Jovanovic T et al (2007) Veterans seeking treatment for posttraumatic stress disorder: what about comorbid chronic pain? J Rehabil Res Dev 44:153–166
Moeller-Bertram T, Keltner J, Strigo IA (2012) Pain and post traumatic stress disorder – review of clinical and experimental evidence. Neuropharmacology 62:586–597
Boudreaux E, Kilpatrick G, Resnick HS et al (1998) Criminal victimization, posttraumatic stress disorder, and comorbid psychopathology among a community sample of women. J Trauma Stress 11:665–678
Swart S, Wildschut M, Draijer N et al (2020) Dissociative subtype of posttraumatic stress disorder or PTSD with comorbid dissociative disorders: comparative evaluation of clinical profiles. Psychol Trauma 12:38–45
Britvić D, Antičević V, Kaliterna M et al (2015) Comorbidities with Posttraumatic Stress Disorder (PTSD) among combat veterans: 15 years postwar analysis. Int J Clin Health Psychol 15:81–92
Pace TW, Heim CM (2011) A short review on the psychoneuroimmunology of posttraumatic stress disorder: from risk factors to medical comorbidities. Brain Behav Immun 25:6–13
Xu Y, Vandeleur C, Müller M et al (2021) Retrospectively assessed trajectories of PTSD symptoms and their subsequent comorbidities. J Psychiatr Res 136:71–79
McFarlane AC, Bookless C (2001) The effect of PTSD on interpersonal relationships: issues for emergency service workers. Sex Relatsh Ther 16:261–267
Laffaye C, Cavella S, Drescher K et al (2008) Relationships among PTSD symptoms, social support, and support source in veterans with chronic PTSD. J Trauma Stress 21:394–401
Fox J, Desai MM, Britten K et al (2012) Mental-health conditions, barriers to care, and productivity loss among officers in an urban police department. Conn Med 76:525–531
Milligan-Saville J, Choi I, Deady M et al (2018) The impact of trauma exposure on the development of PTSD and psychological distress in a volunteer fire service. Psychiatry Res 270:1110–1115
Chopko BA, Palmieri PA, Adams RE (2018) Relationships among traumatic experiences, PTSD, and posttraumatic growth for police officers: a path analysis. Psychol Trauma 10:183–189
Dams J, Rimane E, Steil R et al (2020) Health-related quality of life and costs of posttraumatic stress disorder in adolescents and young adults in Germany. Front Psychiatry 11:697
Ehlers A, Clark DM (2000) A cognitive model of posttraumatic stress disorder. Behav Res Ther 38:319–345
Engelhard IM, Macklin ML, McNally RJ et al (2001) Emotion- and intrusion-based reasoning in Vietnam veterans with and without chronic posttraumatic stress disorder. Behav Res Ther 39:1339–1348
Engelhard IM, Hout MA van den, Arntz A et al (2002) A longitudinal study of “intrusion-based reasoning” and posttraumatic stress disorder after exposure to a train disaster. Behav Res Ther 40:1415–1424
Fortier MA, DiLillo D, Messman-Moore TL et al (2009) Severity of child sexual abuse and revictimization: the mediating role of coping and trauma symptoms. Psychol Women Q 33:308–320
Bistricky SL, Gallagher MW, Roberts CM et al (2017) Frequency of interpersonal trauma types, avoidant attachment, self-compassion, and interpersonal competence: a model of persisting posttraumatic symptoms. J Aggress Maltreat Trauma 26:608–625
Campbell SB, Renshaw KD, Kashdan TB et al (2017) A daily diary study of posttraumatic stress symptoms and romantic partner accommodation. Behav Ther 48:222–234
Lawrence JW, Fauerbach J, Munster A (1996) Early avoidance of traumatic stimuli predicts chronicity of intrusive thoughts following burn injury. Behav Res Ther 34:643–646
Boeding SE, Paprocki CM, Baucom DH et al (2013) Let me check that for you: symptom accommodation in romantic partners of adults with obsessive–compulsive disorder. Behav Res Ther 51:316–322
Eisma MC, Stroebe MS, Schut HA et al (2013) Avoidance processes mediate the relationship between rumination and symptoms of complicated grief and depression following loss. J Abnorm Psychol 122:961–970
Rapee RM, Peters L, Carpenter L et al (2015) The Yin and Yang of support from significant others: influence of general social support and partner support of avoidance in the context of treatment for social anxiety disorder. Behav Res Ther 69:40–47
Belleville G, Guay S, Marchand A (2011) Persistence of sleep disturbances following cognitive-behavior therapy for posttraumatic stress disorder. J Psychosom Res 70:318–327
Liempt S van (2012) Sleep disturbances and PTSD: a perpetual circle? Eur J Psychotraumatol 3:19142
Jaoude P, Vermont LN, Porhomayon J et al (2015) Sleep-disordered breathing in patients with post-traumatic stress disorder. Ann Am Thorac Soc 12:259–268
Wyk M van, Thomas KG, Solms M et al (2016) Prominence of hyperarousal symptoms explains variability of sleep disruption in posttraumatic stress disorder. Psychol Trauma 8:688–696
Hurtado-Alvarado G, Domínguez-Salazar E, Pavon L et al (2016) Blood-brain barrier disruption induced by chronic sleep loss: low-grade inflammation may be the link. J Immunol Res 2016:4576012
Groer MW, Kane B, Williams SN et al (2015) Relationship of PTSD symptoms with combat exposure, stress, and inflammation in American soldiers. Biol Res Nurs 17:303–310
Loupy KM, Lowry CA (2019) Posttraumatic stress disorder and the gut microbiome. In: The Oxford Handbook of the Microbiome-Gut-Brain Axis. Oxford University Press, Oxford
Langgartner D, Lowry CA, Reber SO (2019) Old Friends, immunoregulation, and stress resilience. Pflugers Arch 471:237–269
Kim TD, Lee S, Yoon S (2020) Inflammation in post-traumatic stress disorder (PTSD): a review of potential correlates of PTSD with a neurological perspective. Antioxidants (Basel) 9:107
Bersani FS, Mellon SH, Lindqvist D et al (2020) Novel pharmacological targets for combat PTSD – metabolism, inflammation, the gut microbiome, and mitochondrial dysfunction. Mil Med 185:311–318
Lev-Wiesel R (2007) Intergenerational transmission of trauma across three generations: a preliminary study. Qual Soc Work Res Pract 6:75–94
Dekel R, Goldblatt H (2008) Is there intergenerational transmission of trauma? The case of combat veterans’ children. Am J Orthop 78:281–289
Aguiar W, Halseth R (2015) Aboriginal Peoples and Historic Trauma: The Processes of Intergenerational Transmission. National Collaborating Centre for Aboriginal Health. Prince George, BC
Yehuda R, Lehrner A (2018) Intergenerational transmission of trauma effects: putative role of epigenetic mechanisms. World Psychiatry 17:243–257
Lünnemann M, Van der Horst F, Prinzie P et al (2019) The intergenerational impact of trauma and family violence on parents and their children. Child Abuse Negl 96:104134
Anderson RE, Edwards L-J, Silver KE et al (2018) Intergenerational transmission of child abuse: predictors of child abuse potential among racially diverse women residing in domestic violence shelters. Child Abuse Negl 85:80–90
Hoffart R, Jones NA (2018) Intimate partner violence and intergenerational trauma among Indigenous women. Int Crim Justice Rev 28:25–44
Menzies P (2010) Intergenerational trauma from a mental health perspective. Native Social Work Journal 7:63–85
Başoǧlu M, Kiliç C, Şalcioǧlu E et al (2004) Prevalence of posttraumatic stress disorder and comorbid depression in earthquake survivors in Turkey: an epidemiological study. J Trauma Stress 17:133–141
Salcioglu E, Basoglu M, Livanou M (2007) Post-traumatic stress disorder and comorbid depression among survivors of the 1999 earthquake in Turkey. Disasters 31:115–129
Adams SW, Bowler RM, Russell K et al (2019) PTSD and comorbid depression: social support and self-efficacy in World Trade Center tower survivors 14–15 years after 9/11. Psychol Trauma Theory Res Pract Policy 11:156–164
Campbell DG, Felker BL, Liu C-F et al (2007) Prevalence of depression–PTSD comorbidity: implications for clinical practice guidelines and primary care-based interventions. J Gen Intern Med 22:711–718
Panagioti M, Gooding P, Tarrier N (2009) Post-traumatic stress disorder and suicidal behavior: a narrative review. Clin Psychol Rev 29:471–482
Krysinska K, Lester D (2010) Post-traumatic stress disorder and suicide risk: a systematic review. Arch Suicide Res 14:1–23
Panagioti M, Gooding PA, Tarrier N (2012) A meta-analysis of the association between posttraumatic stress disorder and suicidality: the role of comorbid depression. Compr Psychiatry 53:915–930
Zatti C, Rosa V, Barros A et al (2017) Childhood trauma and suicide attempt: a meta-analysis of longitudinal studies from the last decade. Psychiatry Res 256:353–358
Panagioti M, Gooding PA, Triantafyllou K et al (2015) Suicidality and posttraumatic stress disorder (PTSD) in adolescents: a systematic review and meta-analysis. Soc Psychiatry Psychiatr Epidemiol 50:525–537
Fox V, Dalman C, Dal H et al (2021) Suicide risk in people with post-traumatic stress disorder: a cohort study of 3.1 million people in Sweden. J Affect Disord 279:609–616
Charak R, Armour C, Elklit A et al (2014) Factor structure of PTSD, and relation with gender in trauma survivors from India. Eur J Psychotraumatol 5:25547
Meer CA van der, Bakker A, Smit AS et al (2017) Gender and age differences in trauma and PTSD among Dutch treatment-seeking police officers. J Nerv Ment Dis 205:87–92
Olff M (2017) Sex and gender differences in post-traumatic stress disorder: an update. Eur J Psychotraumatol 8:1351204
Dunlop BW, Kaye JL, Youngner C et al (2014) Assessing treatment-resistant posttraumatic stress disorder: the Emory treatment resistance interview for PTSD (E-TRIP). Behav Sci (Basel) 4:511–527
Imel ZE, Laska K, Jakupcak M et al (2013) Meta-analysis of dropout in treatments for posttraumatic stress disorder. J Consult Clin Psychol 81:394–404
Najavits LM (2015) The problem of dropout from “gold standard” PTSD therapies. F1000prime Rep 7:43
Lewis C, Roberts NP, Gibson S et al (2020) Dropout from psychological therapies for post-traumatic stress disorder (PTSD) in adults: systematic review and meta-analysis. Eur J Psychotraumatol 11:1709709
Simpson TL (2002) Women’s treatment utilization and its relationship to childhood sexual abuse history and lifetime PTSD. Subst Abus 23:17–30
Najavits LM, Sullivan TP, Schmitz M et al (2004) Treatment utilization by women with PTSD and substance dependence. Am J Addict 13:215–224
Peltan JR, Cellucci T (2011) Childhood sexual abuse and substance abuse treatment utilization among substance-dependent incarcerated women. J Subst Abus Treat 41:215–224
Nobles CJ, Valentine SE, Zepeda ED et al (2017) Usual course of treatment and predictors of treatment utilization for patients with posttraumatic stress disorder. J Clin Psychiatry 78:e559–e566
Artime TM, Buchholz KR, Jakupcak M (2019) Mental health symptoms and treatment utilization among trauma-exposed college students. Psychol Trauma Theory Res Pract Policy 11:274–282
Hoge CW, Grossman SH, Auchterlonie JL et al (2014) PTSD treatment for soldiers after combat deployment: low utilization of mental health care and reasons for dropout. Psychiatr Serv 65:997–1004
Goetter EM, Bui E, Ojserkis RA et al (2015) A systematic review of dropout from psychotherapy for posttraumatic stress disorder among Iraq and Afghanistan combat veterans. J Trauma Stress 28:401–409
Schottenbauer MA, Glass CR, Arnkoff DB et al (2008) Nonresponse and dropout rates in outcome studies on PTSD: review and methodological considerations. Psychiatry 71:134–168
Libby DJ, Pilver CE, Desai R (2012) Complementary and alternative medicine in VA specialized PTSD treatment programs. Psychiatr Serv 63:1134–1136
Eisenberg DM, Davis RB, Ettner SL et al (1998) Trends in alternative medicine use in the United States, 1990-1997: results of a follow-up national survey. JAMA 280:1569–1575
Kessler RC, Davis RB, Foster DF et al (2001) Long-term trends in the use of complementary and alternative medical therapies in the United States. Ann Intern Med 135:262–268
Barnes PM, Powell-Griner E, McFann K et al (2004) Complementary and alternative medicine use among adults: United States, 2002. In: Seminars in integrative medicine. Elsevier, pp 54–71
Barnes PM, Bloom B, Nahin RL (2008) Complementary and alternative medicine use among adults and children; United States, 2007. Natl Health Stat Report 10(12):1–23
Su D, Li L (2011) Trends in the use of complementary and alternative medicine in the United States: 2002–2007. J Health Care Poor Underserved 22:296–310
Clarke TC, Black LI, Stussman BJ et al (2015) Trends in the use of complementary health approaches among adults: United States, 2002–2012. Natl Health Stat Report 79:1–16
Williams JW Jr, Gierisch JM, McDuffie J et al (2012) An overview of complementary and alternative medicine therapies for anxiety and depressive disorders: supplement to efficacy of complementary and alternative medicine therapies for posttraumatic stress disorder. Department of Veterans Affairs, Washington, DC
Hemmings SM, Malan-Muller S, Heuvel LL van den et al (2017) The microbiome in posttraumatic stress disorder and trauma-exposed controls: an exploratory study. Psychosom Med 79:936–946
Malan-Muller S, Valles-Colomer M, Raes J et al (2018) The gut microbiome and mental health: implications for anxiety-and trauma-related disorders. OMICS 22:90–107
Hoisington AJ, Billera DM, Bates KL et al (2018) Exploring service dogs for rehabilitation of veterans with PTSD: a microbiome perspective. Rehabil Psychol 63:575–587
Bajaj JS, Sikaroodi M, Fagan A et al (2019) Posttraumatic stress disorder is associated with altered gut microbiota that modulates cognitive performance in veterans with cirrhosis. Am J Physiol Gastrointest Liver Physiol 317:G661–G669
Nikolova VL, Hall MR, Hall LJ et al (2021) Perturbations in gut microbiota composition in psychiatric disorders: a review and meta-analysis. JAMA Psychiatry 78:1343–1354
Malan-Muller S, Valles-Colomer M, Foxx CL et al (2022) Exploring the relationship between the gut microbiome and mental health outcomes in a posttraumatic stress disorder cohort relative to trauma-exposed controls. Eur Neuropsychopharmacol 56:24–38
McGowan I (2019) The economic burden of PTSD. A brief review of salient literature. Int J Psychiatry Med 1:20–26
Ferry FR, Brady SE, Bunting BP et al (2015) The economic burden of PTSD in Northern Ireland. J Trauma Stress 28:191–197
McCrone P, Knapp M, Cawkill P (2003) Posttraumatic stress disorder (PTSD) in the Armed Forces: health economic considerations. J Trauma Stress 16:519–522
Surís A, Lind L, Kashner TM et al (2004) Sexual assault in women veterans: an examination of PTSD risk, health care utilization, and cost of care. Psychosom Med 66:749–756
Chan D, Cheadle AD, Reiber G et al (2009) Health care utilization and its costs for depressed veterans with and without comorbid PTSD symptoms. Psychiatr Serv 60:1612–1617
McGeary D, Moore M, Vriend CA et al (2011) The evaluation and treatment of comorbid pain and PTSD in a military setting: an overview. J Clin Psychol Med Settings 18:155–163
Vyas KJ, Fesperman SF, Nebeker BJ et al (2016) Preventing PTSD and depression and reducing health care costs in the military: a call for building resilience among service members. Mil Med 181:1240–1247
Hardner K, Wolf MR, Rinfrette ES (2018) Examining the relationship between higher educational attainment, trauma symptoms, and internalizing behaviors in child sexual abuse survivors. Child Abuse Negl 86:375–383
Bothe T, Jacob J, Kröger C et al (2020) How expensive are post-traumatic stress disorders? Estimating incremental health care and economic costs on anonymised claims data. Eur J Health Econ 21:917–930
Tan SY, Yip A (2018) Hans Selye (1907–1982): founder of the stress theory. Singap Med J 59:170
Selye H (1936) A syndrome produced by diverse nocuous agents. Nature 138:32–32
Del Giudice M, Buck CL, Chaby LE et al (2018) What is stress? A systems perspective. Integr Comp Biol 58:1019–1032
Gottesman II, Gould TD (2003) The endophenotype concept in psychiatry: etymology and strategic intentions. Am J Psychiatry 160:636–645
Beauchaine TP, Constantino JN (2017) Redefining the endophenotype concept to accommodate transdiagnostic vulnerabilities and etiological complexity. Biomark Med 11:769–780
Mullins LJ, Mullins JJ (2004) Insights from the rat genome sequence. Genome Biol 5:1–3
Gibbs RA, Pachter L (2004) Genome sequence of the Brown Norway rat yields insights into mammalian evolution. Nature 428:493–521
Tabakoff B, Hoffman PL (2000) Animal models in alcohol research. Alcohol Res Health 24:77
Van Den Buuse M, Garner B, Gogos A et al (2005) Importance of animal models in schizophrenia research. Aust N Z J Psychiatry 39:550–557
Mogil JS, Davis KD, Derbyshire SW (2010) The necessity of animal models in pain research. Pain 151:12–17
Swearengen JR (2012) Biodefense research methodology and animal models. CRC Press, Boca Raton, Florida
Abdullahi A, Amini-Nik S, Jeschke M (2014) Animal models in burn research. Cell Mol Life Sci 71:3241–3255
Budhu S, Wolchok J, Merghoub T (2014) The importance of animal models in tumor immunity and immunotherapy. Curr Opin Genet Dev 24:46–51
Azrin N, Hopwood J, Powell J (1967) A rat chamber and electrode procedure for avoidance conditioning 1. J Exp Anal Behav 10:291–298
Skinner B, Campbell S (1947) An automatic shocking-grid apparatus for continuous use. J Comp Physiol Psychol 40:305–37
Sloane H (1964) Scramble patterns and escape learning. J Exp Anal Behav 7:336
Ulrich RE, Azrin NH (1962) Reflexive fighting in response to aversive stimulation 1. J Exp Anal Behav 5:511–520
Silver MP, Schoenfeld WN, Snapper AG et al (1964) Impedance-voltage functions in the white rat with chronic body electrode implants. Psychon Sci 1:61–62
Weiss J (1967) A tail electrode for unrestrained rats. J Exp Anal Behav 10:85–86
Hall RD, Clayton RJ, Mark RG (1966) A device for the partial restraint of rats in operant conditioning studies. J Exp Anal Behav 9:143–145
Paré WP, Glavin GB (1986) Restraint stress in biomedical research: a review. Neurosci Biobehav Rev 10:339–370
Seewoo BJ, Hennessy LA, Feindel KW et al (2020) Validation of chronic restraint stress model in young adult rats for the study of depression using longitudinal multimodal MR imaging. Eneuro 7:ENEURO.0113-20.2020
Clutton-Brock J (1960) Some pain threshold studies with particular reference to thiopentone. Anaesthesia 15:71–72
Spiaggia A, Bodnar RJ, Kelly DD et al (1979) Opiate and non-opiate mechanisms of stress-induced analgesia: cross-tolerance between stressors. Pharmacol Biochem Behav 10:761–765
Grau JW, Hyson RL, Maier SF et al (1981) Long-term stress-induced analgesia and activation of the opiate system. Science 213:1409–1411
Maier SF, Sherman JE, Lewis JW et al (1983) The opioid/nonopioid nature of stress-induced analgesia and learned helplessness. J Exp Psychol Anim Behav Process 9:80–90
Drugan RC, Ader DN, Maier SF (1985) Shock controllability and the nature of stress-induced analgesia. Behav Neurosci 99:791–801
Maier SF (1986) Stressor controllability and stress-induced analgesia. Ann N Y Acad Sci 467:55–72
Maier SF, Watkins LR (1991) Conditioned and unconditioned stress-induced analgesia: stimulus preexposure and stimulus change. Anim Learn Behav 19:295–304
Grisel JE, Fleshner M, Watkins LR et al (1993) Opioid and nonopioid interactions in two forms of stress-induced analgesia. Pharmacol Biochem Behav 45:161–172
Butler RK, Finn DP (2009) Stress-induced analgesia. Prog Neurobiol 88:184–202
Heinke B, Gingl E, Sandkühler J (2011) Multiple targets of μ-opioid receptor-mediated presynaptic inhibition at primary afferent Aδ-and C-fibers. J Neurosci 31:1313–1322
Koga A, Fujita T, Piao L-H et al (2019) Inhibition by O-desmethyltramadol of glutamatergic excitatory transmission in adult rat spinal substantia gelatinosa neurons. Mol Pain 15:1744806918824243
Jones TL, Sweitzer SM, Wilson SP et al (2003) Afferent fiber-selective shift in opiate potency following targeted opioid receptor knockdown. Pain 106:365–371
Ikoma M, Kohno T, Baba H (2007) Differential presynaptic effects of opioid agonists on Aδ-and C-afferent glutamatergic transmission to the spinal dorsal horn. J Neurosci 107:807–812
Lu Y, Sweitzer SM, Laurito CE et al (2004) Differential opioid inhibition of C-and Aδ-fiber mediated thermonociception after stimulation of the nucleus raphe magnus. Anesth Analg 98:414–419
Brederson J-D, Honda CN (2015) Primary afferent neurons express functional delta opioid receptors in inflamed skin. Brain Res 1614:105–111
Hohmann AG, Suplita RL, Bolton NM et al (2005) An endocannabinoid mechanism for stress-induced analgesia. Nature 435:1108–1112
Suplita RL II, Gutierrez T, Fegley D et al (2006) Endocannabinoids at the spinal level regulate, but do not mediate, nonopioid stress-induced analgesia. Neuropharmacology 50:372–379
Rash JA, Aguirre-Camacho A, Campbell TS (2014) Oxytocin and pain: a systematic review and synthesis of findings. Clin J Pain 30:453–462
Van der Kolk B, Greenberg M, Boyd H et al (1985) Inescapable shock, neurotransmitters, and addiction to trauma: toward a psychobiology of post traumatic stress. Biol Psychiatry 20:314–325
Koba T, Kodama Y, Shimizu K et al (2001) Persistent behavioural changes in rats following inescapable shock stress: a potential model of posttraumatic stress disorder. World J Biol Psychiatry 2:34–37
Thornton JW, Jacobs PD (1971) Learned helplessness in human subjects. J Exp Psychol 87:367–372
Seligman ME (1972) Learned helplessness. Annu Rev Med 23:407–412
Seligman ME, Beagley G (1975) Learned helplessness in the rat. J Comp Physiol Psychol 88:534–541
Maier SF, Seligman ME (1976) Learned helplessness: theory and evidence. J Exp Psychol Gen 105:3–46
Maier SF, Jackson RL (1979) Learned helplessness: all of us were right (and wrong): inescapable shock has multiple effects. In: Psychology of Learning and Motivation. Elsevier, pp 155–218
Jackson RL, Maier SF, Coon DJ (1979) Long-term analgesic effects of inescapable shock and learned helplessness. Science 206:91–93
Vollmayr B, Henn FA (2001) Learned helplessness in the rat: improvements in validity and reliability. Brain Res Protocol 8:1–7
Dess NK, Minor TR, Brewer J (1989) Suppression of feeding and body weight by inescapable shock: modulation by quinine adulteration, stress reinstatement, and controllability. Physiol Behav 45:975–983
Cassens G, Roffman M, Kuruc A et al (1980) Alterations in brain norepinephrine metabolism induced by environmental stimuli previously paired with inescapable shock. Science 209:1138–1140
Maier SF, Davies S, Grau JW et al (1980) Opiate antagonists and long-term analgesic reaction induced by inescapable shock in rats. J Comp Physiol Psychol 94:1172–1183
Drugan RC, Maier SF (1983) Analgesic and opioid involvement in the shock-elicited activity and escape deficits produced by inescapable shock. Learn Motiv 14:30–47
Stuckey J, Marra S, Minor T et al (1989) Changes in mu opiate receptors following inescapable shock. Brain Research 476:167–169
Li B, Yang C-J, Yue N et al (2013) Clomipramine reverses hypoalgesia/hypoesthesia and improved depressive-like behaviors induced by inescapable shock in rats. Neurosci Lett 541:227–232
Will MJ, Watkins LR, Maier SF (1998) Uncontrollable stress potentiates morphine’s rewarding properties. Pharmacol Biochem Behav 60:655–664
Weiss J, Bailey W, Pohorecky L et al (1980) Stress-induced depression of motor activity correlates with regional changes in brain norepinephrine but not in dopamine. Neurochem Res 5:9–22
Moraska A, Fleshner M (2001) Voluntary physical activity prevents stress-induced behavioral depression and anti-KLH antibody suppression. Am J Phys Regul Integr Comp Phys 281:R484–R489
Greenwood BN, Foley TE, Day HE et al (2003) Freewheel running prevents learned helplessness/behavioral depression: role of dorsal raphe serotonergic neurons. J Neurosci 23:2889–2898
Vollmayr B, Gass P (2013) Learned helplessness: unique features and translational value of a cognitive depression model. Cell Tissue Res 354:171–178
Landgraf D, Long J, Der-Avakian A et al (2015) Dissociation of learned helplessness and fear conditioning in mice: a mouse model of depression. PLoS One 10:e0125892
Cheng Y, Desse S, Martinez A et al (2018) TNFα disrupts blood brain barrier integrity to maintain prolonged depressive-like behavior in mice. Brain Behav Immun 69:556–567
Daut RA, Ravenel JR, Watkins LR et al (2020) The behavioral and neurochemical effects of an inescapable stressor are time of day dependent. Stress 23:405–416
Biederman GB, Furedy JJ (1973) Preference-for-signaled-shock phenomenon: effects of shock modifiability and light reinforcement. J Exp Psychol 100:380
Kelsey JE (1977) Escape acquisition following inescapable shock in the rat. Anim Learn Behav 5:83–92
Jackson RL, Maier SF, Rapaport PM (1978) Exposure to inescapable shock produces both activity and associative deficits in the rat. Learn Motiv 9:69–98
Nick A, Alexander Z, others (1990) Handling habituation and ehlordiazepoxide have different effects on GABA and 5-HT function in the frontal cortex and hippocampus. Eur J Pharmacol 190:229–234
Petty F, Kramer G, Wilson L (1992) Prevention of learned helplessness: in vivo correlation with cortical serotonin. Pharmacol Biochem Behav 43:361–367
Paré WP (1996) Enhanced retrieval of unpleasant memories influenced by shock controllability, shock sequence, and rat strain. Biological Psychiatry 39:808–813
Campisi J, Leem TH, Fleshner M (2003) Stress-induced extracellular Hsp72 is a functionally significant danger signal to the immune system. Cell Stress Chaperones 8:272
Campisi J, Fleshner M (2003) Role of extracellular HSP72 in acute stress-induced potentiation of innate immunity in active rats. J Appl Physiol 94:43–52
Kirk RC, Blampied NM (1985) Activity during inescapable shock and subsequent escape avoidance learning: female and male rats. N Z J Psychol 14:9–14
Jenkins J, Williams P, Kramer G et al (2000) 249. The effects of gender and the estrous cycle on learned helplessness in the rat. Biol Psychiatry 47:S76
Jenkins JA, Williams P, Kramer GL et al (2001) The influence of gender and the estrous cycle on learned helplessness in the rat. Biol Psychol 58:147–158
Nickerson M, Kennedy SL, Johnson JD et al (2006) Sexual dimorphism of the intracellular heat shock protein 72 response. J Appl Physiol (1985) 101:566–575
Fonken LK, Frank MG, Gaudet AD et al (2018) Neuroinflammatory priming to stress is differentially regulated in male and female rats. Brain Behav Immun 70:257–267
Baratta MV, Leslie NR, Fallon IP et al (2018) Behavioural and neural sequelae of stressor exposure are not modulated by controllability in females. Eur J Neurosci 47:959–967
Baratta MV, Gruene TM, Dolzani SD et al (2019) Controllable stress elicits circuit-specific patterns of prefrontal plasticity in males, but not females. Brain Struct Funct 224:1831–1843
Tanner MK, Fallon IP, Baratta MV et al (2019) Voluntary exercise enables stress resistance in females. Behav Brain Res 369:111923
Vul’fson S (1897) O psikhicheskom vliianii v rabote sliunnykh zhelez [On psychic influence in the work of the salivary glands]. Trudy obshchestva russkikh vrachei 65:110–113
Minor TR, LoLordo VM (1984) Escape deficits following inescapable shock: the role of contextual odor. J Exp Psychol Anim Behav Process 10:168–181
Minor TR, Jackson RL, Maier SF (1984) Effects of task-irrelevant cues and reinforcement delay on choice-escape learning following inescapable shock: evidence for a deficit in selective attention. J Exp Psychol Anim Behav Process 10:543–556
Maier SF (1990) Role of fear in mediating shuttle escape learning deficit produced by inescapable shock. J Exp Psychol Anim Behav Process 16:137–149
Maier SF, Watkins LR (2005) Stressor controllability and learned helplessness: the roles of the dorsal raphe nucleus, serotonin, and corticotropin-releasing factor. Neurosci Biobehav Rev 29:829–841
Chen C-FF, Barnes DC, Wilson DA (2011) Generalized vs. stimulus-specific learned fear differentially modifies stimulus encoding in primary sensory cortex of awake rats. J Neurophysiol 106:3136–3144
Ghosh S, Chattarji S (2015) Neuronal encoding of the switch from specific to generalized fear. Nat Neurosci 18:112–120
Harris JD (1943) Studies on Nonassociative Factors Inherent in conditioning. Williams & Wilkins
Mackintosh N (1974) Classical conditioning: basic operations. The psychology of animal learning, pp 8–40
Kamprath K, Wotjak CT (2004) Nonassociative learning processes determine expression and extinction of conditioned fear in mice. Learn Mem 11:770–786
Perusini JN, Meyer EM, Long VA et al (2016) Induction and expression of fear sensitization caused by acute traumatic stress. Neuropsychopharmacology 41:45–57
Servatius RJ, Ottenweller JE, Natelson BH (1995) Delayed startle sensitization distinguishes rats exposed to one or three stress sessions: further evidence toward an animal model of PTSD. Biol Psychiatry 38:539–546
Mirshekar M, Abrari K, Goudarzi I et al (2013) Systemic administrations of β-estradiol alleviate both conditioned and sensitized fear responses in an ovariectomized rat model of post-traumatic stress disorder. Neurobiol Learn Mem 102:12–19
Thompson R, Strong P, Clark P et al (2014) Repeated fear-induced diurnal rhythm disruptions predict PTSD-like sensitized physiological acute stress responses in F 344 rats. Acta Physiol (Oxf) 211:447–465
Rajbhandari AK, Baldo BA, Bakshi VP (2015) Predator stress-induced CRF release causes enduring sensitization of basolateral amygdala norepinephrine systems that promote PTSD-like startle abnormalities. J Neurosci 35:14270–14285
Maier SF (1990) Diazepam modulation of stress-induced analgesia depends on the type of analgesia. Behav Neurosci 104:339–347
Maier SF, Watkins LR (1998) Stressor controllability, anxiety, and serotonin. Cognit Ther Res 22:595–613
Christianson JP, Benison AM, Jennings J et al (2008) The sensory insular cortex mediates the stress-buffering effects of safety signals but not behavioral control. J Neurosci 28:13703–13711
Weiss JM (1968) Effects of coping responses on stress. J Comp Physiol Psychol 65:251–260
Maier SF, Seligman MEP, Solomon RL (1969) Pavlovian fear conditioning and learned helplessness: Effects on escape and avoidance behavior of (a) the CS-US contingency and (b) the independence of the US and voluntary responding. In Campbell, B.A., and Church, R.M. (Eds.), Punishment. Appleton-Century-Crofts, New York, pp 299–343
Traini C, Evangelista S, Girod V et al (2016) Changes of excitatory and inhibitory neurotransmitters in the colon of rats underwent to the wrap partial restraint stress. Neurogastroenterol Motil 28:1172–1185
Davidson JR, Stein DJ, Shalev AY et al (2004) Posttraumatic stress disorder: acquisition, recognition, course, and treatment. J Neuropsychiatr Clin Neurosci 16:135–147
Jeong M-J, Lee C, Sung K et al (2020) Fear response-based prediction for stress susceptibility to PTSD-like phenotypes. Mol Brain 13:1–9
Watkins L, Drugan R, Hyson R et al (1984) Opiate and non-opiate analgesia induced by inescapable tail-shock: effects of dorsolateral funiculus lesions and decerebration. Brain Res 291:325–336
Khan S, Liberzon I (2004) Topiramate attenuates exaggerated acoustic startle in an animal model of PTSD. Psychopharmacology 172:225–229
Wang W, Liu Y, Zheng H et al (2008) A modified single-prolonged stress model for post-traumatic stress disorder. Neurosci Lett 441:237–241
Pickens CL, Golden SA, Adams-Deutsch T et al (2009) Long-lasting incubation of conditioned fear in rats. Biol Psychiatry 65:881–886
Pickens CL, Navarre BM, Nair SG (2010) Incubation of conditioned fear in the conditioned suppression model in rats: role of food-restriction conditions, length of conditioned stimulus, and generality to conditioned freezing. Neuroscience 169:1501–1510
Pamplona F, Henes K, Micale V et al (2011) Prolonged fear incubation leads to generalized avoidance behavior in mice. J Psychiatr Res 45:354–360
Estes WK, Skinner BF (1941) Some quantitative properties of anxiety. J Exp Psychol 29:390–400
Masserman JH, Yum K (1946) An analysis of the influence of alcohol on experimental neuroses in cats. Psychosom Med 8:36–52
Conger JJ (1951) The effects of alcohol on conflict behavior in the albino rat. Q J Stud Alcohol 12:1–29
Jacobsen E (1957) The effect of psychotropic drugs under psychic stress. In: Psychotropic drugs. Elsevier Publishing Co, Amsterdam, pp 119–124
Miller NE, Angell JR (1957) Objective techniques for studying motivational effects of drugs on animals. Sympotium on psychotropic drugs
Naess K, Rasmussen EW (1958) Approach-withdrawal responses and other specific behaviour reactions as screening test for tranquillizers. Acta Pharmacol 15:99–114
Geller I, Seifter J (1960) The effects of meprobamate, barbiturates, d-amphetamine and promazine on experimentally induced conflict in the rat. Psychopharmacologia 1:482–492
Latane B, Hothersall D (1972) Social attraction in animals. In: Dodwell PC (ed) New Horizons in Psychology 2. Penguin, Baltimore
File SE, Hyde J (1978) Can social interaction be used to measure anxiety? Br J Pharmacol 62:19–24
Blanchard RJ, Blanchard DC (1989) Attack and defense in rodents as ethoexperimental models for the study of emotion. Prog Neuro-Psychopharmacol Biol Psychiatry 13:S3–S14
File SE, Seth P (2003) A review of 25 years of the social interaction test. Eur J Pharmacol 463:35–53
Gong Z-H, Li Y-F, Zhao N et al (2006) Anxiolytic effect of agmatine in rats and mice. Eur J Pharmacol 550:112–116
Lapin IP, Mutovkina LG, Ryzov IV et al (1996) Anxiogenic activity of quinolinic acid and kynurenine in the social interaction test in mice. J Psychopharmacol 10:246–249
Kita A, Furukawa K (2008) Involvement of neurosteroids in the anxiolytic-like effects of AC-5216 in mice. Pharmacol Biochem Behav 89:171–178
File SE, Cheeta S, Akanezi C (2001) Diazepam and nicotine increase social interaction in gerbils: a test for anxiolytic action. Brain Res 888:311–313
Cheeta S, Tucci S, Sandhu J et al (2001) Anxiolytic actions of the substance P (NK1) receptor antagonist L-760735 and the 5-HT1A agonist 8-OH-DPAT in the social interaction test in gerbils. Brain Res 915:170–175
Greenberg GD, Westerhuyzen JA van, Bales KL et al (2012) Is it all in the family? The effects of early social structure on neural–behavioral systems of prairie voles (Microtus ochrogaster). Neuroscience 216:46–56
Lee NS, Goodwin NL, Freitas KE et al (2019) Affiliation, aggression, and selectivity of peer relationships in meadow and prairie voles. Front Behav Neurosci 13:52
Normann M (2020) Investigating the behavioral effects of juvenile stress in the prairie vole model. Northern Illinois University ProQuest Dissertations Publishing
Rivera DS, Lindsay CB, Codocedo JF et al (2018) Long-term, fructose-induced metabolic syndrome-like condition is associated with higher metabolism, reduced synaptic plasticity and cognitive impairment in Octodon degus. Mol Neurobiol 55:9169–9187
Rivera DS, Lindsay CB, Oliva CA et al (2021) A multivariate assessment of age-related cognitive impairment in Octodon degus. Front Integr Neurosci 15:719076
Thor D (1979) Olfactory perception and inclusive fitness. Physiol Psychol 7:303–306
Miczek KA (1979) A new test for aggression in rats without aversive stimulation: differential effects of d-amphetamine and cocaine. Psychopharmacology 60:253–259
File SE, Deakin J, Longden A et al (1979) An investigation of the role of the locus coeruleus in anxiety and agonistic behaviour. Brain Res 169:411–420
File SE, Hyde J, MacLeod N (1979) 5, 7-dihydroxytryptamine lesions of dorsal and median raphe nuclei and performance in the social interaction test of anxiety and in a home-cage aggression test. J Affect Disord 1:115–122
Maier DM, Pohorecky LA (1987) The effect of ethanol treatment on social behavior in male rats. Physiol Behav 13:259–268
Bluthe R-M, Schoenen J, Dantzer R (1990) Androgen-dependent vasopressinergic neurons are involved in social recognition in rats. Brain Res 519:150–157
Dantzer R, Bluthe R-M, Kelley KW (1991) Androgen-dependent vasopressinergic neurotransmission attenuates interleukin-1-induced sickness behavior. Brain Res 557:115–120
Patel HP (2016) Investigating the sensitivity of juvenile social exploration at detecting the affective consequences accompanying chronic neuropathic pain. Mol Pain 12:1744806916656635
Jacobson-Pick S, Audet M-C, Nathoo N et al (2011) Stressor experiences during the juvenile period increase stressor responsivity in adulthood: transmission of stressor experiences. Behav Brain Res 216:365–374
Daut RA, Hartsock MJ, Tomczik AC et al (2019) Circadian misalignment has differential effects on affective behavior following exposure to controllable or uncontrollable stress. Behav Brain Res 359:440–445
Frank MG, Baratta MV, Zhang K et al (2020) Acute stress induces the rapid and transient induction of caspase-1, gasdermin D and release of constitutive IL-1β protein in dorsal hippocampus. Brain Behav Immun 90:70–80
Bilbo SD, Yirmiya R, Amat J et al (2008) Bacterial infection early in life protects against stressor-induced depressive-like symptoms in adult rats. Psychoneuroendocrinology 33:261–269
Christianson JP, Paul ED, Irani M et al (2008) The role of prior stressor controllability and the dorsal raphe nucleus in sucrose preference and social exploration. Behav Brain Res 193:87–93
Christianson JP, Ragole T, Amat J et al (2010) 5-hydroxytryptamine 2C receptors in the basolateral amygdala are involved in the expression of anxiety after uncontrollable traumatic stress. Biol Psychiatry 67:339–345
Christianson JP, Thompson BM, Watkins LR et al (2009) Medial prefrontal cortical activation modulates the impact of controllable and uncontrollable stressor exposure on a social exploration test of anxiety in the rat. Stress 12:445–450
Goshen I, Yirmiya R (2009) Interleukin-1 (IL-1): a central regulator of stress responses. Front Neuroendocrinol 30:30–45
Loupy KM, Cler KE, Marquart BM et al (2021) Comparing the effects of two different strains of mycobacteria, Mycobacterium vaccae NCTC 11659 and M. vaccae ATCC 15483, on stress-resilient behaviors and lipid-immune signaling in rats. Brain Behav Immun 91:212–229
Niesink RJ, Van Ree JM (1982) Short-term isolation increases social interactions of male rats: a parametric analysis. Physiol Behav 29:819–825
Drugan RC, Basile AS, Ha J-H et al (1997) Analysis of the importance of controllable versus uncontrollable stress on subsequent behavioral and physiological functioning. Brain Res Brain Res Protoc 2:69–74
Fleshner M, Maier SF, Lyons DM et al (2011) The neurobiology of the stress-resistant brain. Stress 14:498–502
Rozeske RR, Greenwood BN, Fleshner M et al (2011) Voluntary wheel running produces resistance to inescapable stress-induced potentiation of morphine conditioned place preference. Behav Brain Res 219:378–381
Frank MG, Fonken LK, Dolzani SD et al (2018) Immunization with Mycobacterium vaccae induces an anti-inflammatory milieu in the CNS: attenuation of stress-induced microglial priming, alarmins and anxiety-like behavior. Behav Brain Res 73:352–363
Siegmund A, Wotjak CT (2007) A mouse model of posttraumatic stress disorder that distinguishes between conditioned and sensitised fear. J Psychiatr Res 41:848–860
Golub Y, Mauch CP, Dahlhoff M et al (2009) Consequences of extinction training on associative and non-associative fear in a mouse model of Posttraumatic Stress Disorder (PTSD). Behav Brain Res 205:544–549
McNay E Sprague Dawley. https://www.albany.edu/mcnaylab/sd.html
Pan Y, Zhang W-Y, Xia X et al (2006) Effects of icariin on hypothalamic-pituitary-adrenal axis action and cytokine levels in stressed Sprague-Dawley rats. Biol Pharm Bull 29:2399–2403
Fediuc S, Campbell JE, Riddell MC (2006) Effect of voluntary wheel running on circadian corticosterone release and on HPA axis responsiveness to restraint stress in Sprague-Dawley rats. J Appl Physiol (1985) 100:1867–1875
Shi G, Ku B, Yao H (2007) Effects of jieyuwan on HPA axis and immune system in chronic stress models in rats. Zhongguo Zhong Yao Za Zhi 32:1551–1554
Knaepen L, Rayen I, Charlier TD et al (2013) Developmental fluoxetine exposure normalizes the long-term effects of maternal stress on post-operative pain in Sprague-Dawley rat offspring. PLoS One 8:e57608
Caruso M, McClintock M, Cavigelli S (2014) Temperament moderates the influence of periadolescent social experience on behavior and adrenocortical activity in adult male rats. Horm Behav 66:517–524
Gileta AF, Fitzpatrick CJ, Chitre AS et al (2021) Genetic characterization of outbred Sprague Dawley rats and utility for genome-wide association studies. bioRxiv 412924
White W, Lee C (1998) The development and maintenance of the Crl: CD (SD) IGS BR rat breeding system. Biol Ref Data CD (SD) IGS Rats 8–14
De Boer S, Van der Gugten J, Slangen J (1989) Plasma catecholamine and corticosterone responses to predictable and unpredictable noise stress in rats. Physiol Behav 45:789–795
Muscat R, Willner P (1992) Suppression of sucrose drinking by chronic mild unpredictable stress: a methodological analysis. Neurosci Biobehav Rev 16:507–517
Papp M, Muscat R, Willner P (1993) Subsensitivity to rewarding and locomotor stimulant effects of a dopamine agonist following chronic mild stress. Psychopharmacology (Berl) 110:152–158
Gouirand AM, Matuszewich L (2005) The effects of chronic unpredictable stress on male rats in the water maze. Physiol Behav 86:21–31
Katsnelson A (2014) Male researchers stress out rodents. . Nature doi:10.1038/nature.2014.15106
Sorge RE, Martin LJ, Isbester KA et al (2014) Olfactory exposure to males, including men, causes stress and related analgesia in rodents. Nat Methods 11:629–632
Terashvili MN, Kozak KN, Gebremedhin D et al (2020) Effect of nearby construction activity on endothelial function, sensitivity to nitric oxide, and potassium channel activity in the middle cerebral arteries of rats. J Am Assoc Lab Anim Sci 59:411–422
Dallman MF, Akana SF, Bell ME et al (1999) Warning! Nearby construction can profoundly affect your experiments. Endocrine 11(2):111–113
Bitinas IA (1967) Aggression caused by withdrawal from morphine. [Doctoral dissertation, Western Michigan University], ProQuest Dissertations & Theses Global 1301396
Lal H (1967) Operant control of vocal responding in rats. Psychon Sci 8:35–36
Baker S, Bielajew C (2007) Influence of housing on the consequences of chronic mild stress in female rats. Stress 10:283–293
Azar T, Sharp J, Lawson D (2011) Heart rates of male and female Sprague–Dawley and spontaneously hypertensive rats housed singly or in groups. J Am Assoc Lab Anim Sci 50:175–184
McGrath J, Drummond G, McLachlan E et al (2010) Guidelines for reporting experiments involving animals: the ARRIVE guidelines. Br J Pharmacol 160:1573–1576
Percie du Sert N, Hurst V, Ahluwalia A et al (2020) The ARRIVE guidelines 2.0: updated guidelines for reporting animal research. J Cereb Blood Flow Metab 40:1769–1777
Frank MG, Fonken LK, Watkins LR et al (2020) Acute stress induces chronic neuroinflammatory, microglial and behavioral priming: a role for potentiated NLRP3 inflammasome activation. Brain Behav Immun 89:32–42
Worley NB (2019) Prefrontal circuit selection in stress and resilience. [Doctoral dissertation, Boston College], ProQuest Dissertations & Theses Global 13885882
Horseman ND, Ehret CF (1982) Glucocorticosteroid injection is a circadian zeitgeber in the laboratory rat. Am J Phys 243:R373–R378
Xu R, Liu Z, Zhao Y (1991) A study on the circadian rhythm of glucocorticoid receptor. Neuroendocrinology 53:31–36
Deak T, Nguyen KT, Fleshner M et al (1999) Acute stress may facilitate recovery from a subcutaneous bacterial challenge. Neuroimmunomodulation 6:344–354
Stanojević S, Mitić K, Vujić V et al (2007) The influence of stress and methionine-enkephalin on macrophage functions in two inbred rat strains. Life Sci 80:901–909
Fleshner M, Campisi J, Deak T et al (2002) Acute stressor exposure facilitates innate immunity more in physically active than in sedentary rats. Am J Phys Regul Integr Comp Phys 282:R1680–R1686
Campisi J, Leem TH, Fleshner M (2002) Acute stress decreases inflammation at the site of infection: a role for nitric oxide. Physiol Behav 77:291–299
Campisi J, Leem TH, Greenwood BN et al (2003) Habitual physical activity facilitates stress-induced HSP72 induction in brain, peripheral, and immune tissues. Am J Physiol Regul Integr Comp Physiol 284:R520–R530
Gómez F, De Kloet ER, Armario A (1998) Glucocorticoid negative feedback on the HPA axis in five inbred rat strains. Am J Phys Regul Integr Comp Phys 274:R420–R427
Paré WP (1989) Stress ulcer susceptibility and depression in Wistar Kyoto (WKY) rats. Physiol Behav 46:993–998
Paré WP (1992) Learning behavior, escape behavior, and depression in an ulcer susceptible rat strain. Integr Physiol Behav Sci 27:130–141
Machholz E, Mulder G, Ruiz C et al (2012) Manual restraint and common compound administration routes in mice and rats. J Vis Exp 67:e2771
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Andersen, N.D. et al. (2023). An Integrative Model for Endophenotypes Relevant to Posttraumatic Stress Disorder (PTSD): Detailed Methodology for Inescapable Tail Shock Stress (IS) and Juvenile Social Exploration (JSE). In: Pinna, G. (eds) Translational Methods for PTSD Research. Neuromethods, vol 198. Humana, New York, NY. https://doi.org/10.1007/978-1-0716-3218-5_7
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