Long-term inflammatory pain does not impact exploratory behavior and stress coping strategies in mice.
Journal
Pain
ISSN: 1872-6623
Titre abrégé: Pain
Pays: United States
ID NLM: 7508686
Informations de publication
Date de publication:
01 06 2021
01 06 2021
Historique:
received:
27
07
2020
accepted:
15
12
2020
pubmed:
13
1
2021
medline:
20
5
2021
entrez:
12
1
2021
Statut:
ppublish
Résumé
Pain puts patients at risk for developing psychiatric conditions such as anxiety and depression. Preclinical mouse models of pain-induced affective behavior vary widely in methodology and results, impairing progress towards improved therapeutics. To systematically investigate the effect of long-term inflammatory pain on exploratory behavior and stress coping strategy, we assessed male C57BL/6J mice in the forced swim test (FST), elevated zero maze, and open field test at 4 and 6 weeks postinjection of Complete Freund's Adjuvant, while controlling for testing order and combination. Inflammatory pain did not induce a passive stress coping strategy in the FST and did not reduce exploratory behavior in the elevated zero maze or the open field test. Using systematic correlational analysis and composite behavioral scores, we found no consistent association among measures for mice with or without inflammatory pain. A meta-analysis of similar studies indicated a modest, significant effect of Complete Freund's Adjuvant on exploratory behavior, but not immobility in the FST, and high heterogeneity among effect sizes in all 3 paradigms. Given the urgency for understanding the mechanisms of pain comorbidities and identifying novel therapies, these findings support the reallocation of our limited resources away from such unreliable assays and toward motivated and naturalistic behaviors. Future studies in pain and psychiatric translational research may benefit by considering outcomes beyond binary categorization, quantifying the associations between multiple measured behaviors, and agnostically identifying subtle yet meaningful patterns in behaviors.
Identifiants
pubmed: 33433146
doi: 10.1097/j.pain.0000000000002179
pii: 00006396-202106000-00014
pmc: PMC8119306
mid: NIHMS1656380
doi:
Types de publication
Journal Article
Meta-Analysis
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
1705-1721Subventions
Organisme : NIDA NIH HHS
ID : R01 DA041781
Pays : United States
Organisme : NIDA NIH HHS
ID : R01 DA042499
Pays : United States
Organisme : NIDA NIH HHS
ID : R01 DA045463
Pays : United States
Informations de copyright
Copyright © 2021 International Association for the Study of Pain.
Références
Anderson EM, Gomez D, Caccamise A, McPhail D, Hearing M. Chronic unpredictable stress promotes cell-specific plasticity in prefrontal cortex D1 and D2 pyramidal neurons. Neurobiol Stress 2019;10:100152.
Apkarian AV, Sosa Y, Krauss BR, Thomas PS, Fredrickson BE, Levy RE, Harden RN, Chialvo DR. Chronic pain patients are impaired on an emotional decision-making task. PAIN 2004;108:129–36.
Barthas F, Sellmeijer J, Hugel S, Waltisperger E, Barrot M, Yalcin I. The anterior cingulate cortex is a critical hub for pain-induced depression. Biol Psychiatry 2015;77:236–45.
Bernal-Morales B, Guillén-Ruiz G, Cueto-Escobedo J, Rodríguez-Landa JF, Contreras CM. Sensitivity to diazepam after a single session of forced swim stress in weaning Wistar rats. Acta Pharm 2018;68:381–8.
Biala G, Pekala K, Boguszewska-Czubara A, Michalak A, Kruk-Slomka M, Budzynska B. Behavioral and biochemical interaction between nicotine and chronic unpredictable mild stress in mice. Mol Neurobiol 2017;54:904–21.
Cahill CM, Taylor AMW, Cook C, Ong E, Morón JA, Evans CJ. Does the kappa opioid receptor system contribute to pain aversion? Front Pharmacol 2014;5:253.
Chaudhuri A, Behan PO. Fatigue in neurological disorders. Lancet 2004;363:978–88.
Cheah M, Fawcett JW, Andrews MR. Assessment of thermal pain sensation in rats and mice using the Hargreaves test. Bio Protoc 2017;7:e2506.
Cobos EJ, Portillo-Salido E. “Bedside-to-Bench” behavioral outcomes in animal models of pain: beyond the evaluation of reflexes. Curr Neuropharmacol 2013;11:560–91.
Commons KG, Cholanians AB, Babb JA, Ehlinger DG. The rodent forced swim test measures stress-coping strategy, not depression-like behavior. ACS Chem Neurosci 2017;8:955–60.
Cuthbert BN, Insel TR. Toward the future of psychiatric diagnosis: the seven pillars of RDoC. BMC Med 2013;11:126.
Dantzer R, O'Connor JC, Freund GG, Johnson RW, Kelley KW. From inflammation to sickness and depression: when the immune system subjugates the brain. Nat Rev Neurosci 2008;9:46–56.
Doron R, Lotan D, Versano Z, Benatav L, Franko M, Armoza S, Kately N, Rehavi M. Escitalopram or novel herbal mixture treatments during or following exposure to stress reduce anxiety-like behavior through corticosterone and BDNF modifications. PLoS One 2014;9:e91455.
Feehan AK, Zadina JE. Morphine immunomodulation prolongs inflammatory and postoperative pain while the novel analgesic ZH853 accelerates recovery and protects against latent sensitization. J Neuroinflammation 2019;16:100.
Gonzalez LE, File SE. A five minute experience in the elevated plus-maze alters the state of the benzodiazepine receptor in the dorsal raphe nucleus. J Neurosci 1997;17:1505–11.
Guan S-Y, Zhang K, Wang X-S, Yang L, Feng B, Tian D-D, Gao M-R, Liu S-B, Liu A, Zhao M-G. Anxiolytic effects of polydatin through the blockade of neuroinflammation in a chronic pain mouse model. Mol Pain 2020;16:1744806919900717.
Guo B, Wang J, Yao H, Ren K, Chen J, Yang J, Cai G, Liu H, Fan Y, Wang W, Wu S. Chronic inflammatory pain impairs mGluR5-mediated depolarization-induced suppression of excitation in the anterior cingulate cortex. Cereb Cortex 2018;28:2118–30.
Guo H-L, Xiao Y, Tian Z, Li X-B, Wang D-S, Wang X-S, Zhang Z-W, Zhao M-G, Liu S-B. Anxiolytic effects of sesamin in mice with chronic inflammatory pain. Nutr Neurosci 2016;19:231–6.
Hipólito L, Wilson-Poe A, Campos-Jurado Y, Zhong E, Gonzalez-Romero J, Virag L, Whittington R, Comer SD, Carlton SM, Walker BM, Bruchas MR, Morón JA. Inflammatory pain promotes increased opioid self-administration: role of dysregulated ventral tegmental area μ opioid receptors. J Neurosci 2015;35:12217–31.
Hodes GE, Pfau ML, Purushothaman I, Ahn HF, Golden SA, Christoffel DJ, Magida J, Brancato A, Takahashi A, Flanigan ME, Ménard C, Aleyasin H, Koo JW, Lorsch ZS, Feng J, Heshmati M, Wang M, Turecki G, Neve R, Zhang B, Shen L, Nestler EJ, Russo SJ. Sex differences in nucleus accumbens transcriptome profiles associated with susceptibility versus resilience to subchronic variable stress. J Neurosci 2015;35:16362–76.
Hooten WM. Chronic pain and mental health disorders: shared neural mechanisms, epidemiology, and treatment. Mayo Clin Proc 2016;91:955–70.
Hsu AI, Yttri EA. B-SOiD: an open source unsupervised algorithm for discovery of spontaneous behaviors. bioRxiv 2019:770271.
Jindal A, Mahesh R, Bhatt S. Etazolate rescues behavioral deficits in chronic unpredictable mild stress model: modulation of hypothalamic-pituitary-adrenal axis activity and brain-derived neurotrophic factor level. Neurochem Int 2013;63:465–75.
Johnson A, Rainville JR, Rivero-Ballon GN, Dhimitri K, Hodes GE. Testing the limits of sex differences using variable stress. Neuroscience 2020;S0306-4522(19)-3088-9. Epub ahead of print.
Knight B, Katz DR, Isenberg DA, Ibrahim MA, Le Page S, Hutchings P, Schwartz RS, Cooke A. Induction of adjuvant arthritis in mice. Clin Exp Immunol 1992;90:459–65.
Koob GF. Neurobiology of opioid addiction: opponent process, hyperkatifeia, and negative reinforcement. Biol Psychiatry 2020;87:44–53.
Laumet G, Edralin JD, Dantzer R, Heijnen CJ, Kavelaars A. CD3+ T cells are critical for the resolution of comorbid inflammatory pain and depression-like behavior. Neurobiol Pain 2020;7:100043.
Le AM, Lee M, Su C, Zou A, Wang J. AMPAkines have novel analgesic properties in rat models of persistent neuropathic and inflammatory pain. Anesthesiology 2014;121:1080–90.
Letzen JE, Seminowicz DA, Campbell CM, Finan PH. Exploring the potential role of mesocorticolimbic circuitry in motivation for and adherence to chronic pain self-management interventions. Neurosci Biobehav Rev 2019;98:10–17.
Leventopoulos M, Russig H, Feldon J, Pryce CR, Opacka-Juffry J. Early deprivation leads to long-term reductions in motivation for reward and 5-HT1A binding and both effects are reversed by fluoxetine. Neuropharmacology 2009;56:692–701.
Leys LJ, Chu KL, Xu J, Pai M, Yang HS, Robb HM, Jarvis MF, Radek RJ, McGaraughty S. Disturbances in slow-wave sleep are induced by models of bilateral inflammation, neuropathic, and postoperative pain, but not osteoarthritic pain in rats. PAIN 2013;154:1092–102.
Liu Y, Yang L, Yu J, Zhang Y-Q. Persistent, comorbid pain and anxiety can be uncoupled in a mouse model. Physiol Behav 2015;151:55–63.
Luo L, Sun T, Yang L, Liu A, Liu Q-Q, Tian Q-Q, Wang Y, Zhao M-G, Yang Q. Scopoletin ameliorates anxiety-like behaviors in complete Freund's adjuvant-induced mouse model. Mol Brain 2020;13:15.
Maciel IS, Silva RBM, Morrone FB, Calixto JB, Campos MM. Synergistic effects of celecoxib and bupropion in a model of chronic inflammation-related depression in mice. PLoS One 2013;8:e77227.
Massaly N, Copits BA, Wilson-Poe AR, Hipólito L, Markovic T, Yoon HJ, Liu S, Walicki MC, Bhatti DL, Sirohi S, Klaas A, Walker BM, Neve R, Cahill CM, Shoghi KI, Gereau RW, McCall JG, Al-Hasani R, Bruchas MR, Morón JA. Pain-induced negative affect is mediated via recruitment of the nucleus accumbens kappa opioid system. Neuron 2019;102:564–73.e6.
Narita M, Kaneko C, Miyoshi K, Nagumo Y, Kuzumaki N, Nakajima M, Nanjo K, Matsuzawa K, Yamazaki M, Suzuki T. Chronic pain induces anxiety with concomitant changes in opioidergic function in the amygdala. Neuropsychopharmacology 2006;31:739–50.
Nasca C, Menard C, Hodes G, Bigio B, Pena C, Lorsch Z, Zelli D, Ferris A, Kana V, Purushothaman I, Dobbin J, Nassim M, DeAngelis P, Merad M, Rasgon N, Meaney M, Nestler EJ, McEwen BS, Russo SJ. Multidimensional predictors of susceptibility and resilience to social defeat stress. Biol Psychiatry 2019;86:483–91.
Nasca C, Xenos D, Barone Y, Caruso A, Scaccianoce S, Matrisciano F, Battaglia G, Mathé AA, Pittaluga A, Lionetto L, Simmaco M, Nicoletti F. L-acetylcarnitine causes rapid antidepressant effects through the epigenetic induction of mGlu2 receptors. Proc Natl Acad Sci USA 2013;110:4804–9.
Navratilova E, Porreca F. Reward and motivation in pain and pain relief. Nat Neurosci 2014;17:1304–12.
di Nuzzo L, Orlando R, Tognoli C, Di Pietro P, Bertini G, Miele J, Bucci D, Motolese M, Scaccianoce S, Caruso A, Mauro G, De Lucia C, Battaglia G, Bruno V, Fabene PF, Nicoletti F. Antidepressant activity of fingolimod in mice. Pharmacol Res Perspect 2015;3:e00135.
O'Connor JC, Lawson MA, André C, Moreau M, Lestage J, Castanon N, Kelley KW, Dantzer R. Lipopolysaccharide-induced depressive-like behavior is mediated by indoleamine 2,3-dioxygenase activation in mice. Mol Psychiatry 2009;14:511–22.
Okun A, McKinzie DL, Witkin JM, Remeniuk B, Husein O, Gleason SD, Oyarzo J, Navratilova E, McElroy B, Cowen S, Kennedy JD, Porreca F. Hedonic and motivational responses to food reward are unchanged in rats with neuropathic pain. PAIN 2016;157:2731–8.
Parent AJ, Beaudet N, Beaudry H, Bergeron J, Bérubé P, Drolet G, Sarret P, Gendron L. Increased anxiety-like behaviors in rats experiencing chronic inflammatory pain. Behav Brain Res 2012;229:160–7.
Peña CJ, Smith M, Ramakrishnan A, Cates HM, Bagot RC, Kronman HG, Patel B, Chang AB, Purushothaman I, Dudley J, Morishita H, Shen L, Nestler EJ. Early life stress alters transcriptomic patterning across reward circuitry in male and female mice. Nat Commun 2019;10:5098.
Peng Y-L, Liu Y-N, Liu L, Wang X, Jiang C-L, Wang Y-X. Inducible nitric oxide synthase is involved in the modulation of depressive behaviors induced by unpredictable chronic mild stress. J Neuroinflammation 2012;9:75.
Pitzer C, Kuner R, Tappe-Theodor A. Voluntary and evoked behavioral correlates in inflammatory pain conditions under different social housing conditions. Pain Rep 2016;1:e564.
Pitzer C, La Porta C, Treede R-D, Tappe-Theodor A. Inflammatory and neuropathic pain conditions do not primarily evoke anxiety-like behaviours in C57BL/6 mice. Eur J Pain 2019;23:285–306.
Racine M. Chronic pain and suicide risk: a comprehensive review. Prog Neuropsychopharmacol Biol Psychiatry 2018;87:269–80.
Raison CL, Capuron L, Miller AH. Cytokines sing the blues: inflammation and the pathogenesis of depression. Trends Immunol 2006;27:24–31.
Ramaker MJ, Dulawa SC. Identifying fast-onset antidepressants using rodent models. Mol Psychiatry 2017;22:656–65.
Refsgaard LK, Hoffmann-Petersen J, Sahlholt M, Pickering DS, Andreasen JT. Modelling affective pain in mice: effects of inflammatory hypersensitivity on place escape/avoidance behaviour, anxiety and hedonic state. J Neurosci Methods 2016;262:85–92.
Schwartz N, Temkin P, Jurado S, Lim BK, Heifets BD, Polepalli JS, Malenka RC. Chronic pain. Decreased motivation during chronic pain requires long-term depression in the nucleus accumbens. Science 2014;345:535–42.
Sheahan TD, Siuda ER, Bruchas MR, Shepherd AJ, Mohapatra DP, Gereau RW, Golden JP. Inflammation and nerve injury minimally affect mouse voluntary behaviors proposed as indicators of pain. Neurobiol Pain 2017;2:1–12.
Shi M, Wang J-Y, Luo F. Depression shows divergent effects on evoked and spontaneous pain behaviors in rats. J Pain 2010;11:219–29.
Sun T, Luo L, Tian Q-Q, Wang W-J, Liu Q-Q, Yang L, Zhang K, Zhang W, Zhao M-G, Yang Q. Anxiolytic effects of 8-O-acetyl shanzhiside methylester on acute and chronic anxiety via inflammatory response inhibition and excitatory/inhibitory transmission imbalance. Neurotox Res 2020;38:979–991.
Sun T, Wang J, Li X, Li Y-J, Feng D, Shi W-L, Zhao M-G, Wang J-B, Wu Y-M. Gastrodin relieved complete Freund's adjuvant-induced spontaneous pain by inhibiting inflammatory response. Int Immunopharmacol 2016;41:66–73.
Suurmond R, van Rhee H, Hak T. Introduction, comparison, and validation of Meta-Essentials: a free and simple tool for meta-analysis. Res Synth Methods 2017;8:537–53.
Tang NKY, Beckwith P, Ashworth P. Mental defeat is associated with suicide intent in patients with chronic pain. Clin J Pain 2016;32:411–19.
Thakare VN, Patil RR, Oswal RJ, Dhakane VD, Aswar MK, Patel BM. Therapeutic potential of silymarin in chronic unpredictable mild stress induced depressive-like behavior in mice. J Psychopharmacol (Oxford) 2018;32:223–35.
Tian J, Tian Z, Qin S-L, Zhao P-Y, Jiang X, Tian Z. Anxiolytic-like effects of α-asarone in a mouse model of chronic pain. Metab Brain Dis 2017;32:2119–29.
Urban R, Scherrer G, Goulding EH, Tecott LH, Basbaum AI. Behavioral indices of ongoing pain are largely unchanged in male mice with tissue or nerve injury-induced mechanical hypersensitivity. PAIN 2011;152:990–1000.
Vachon-Presseau E, Roy M, Martel M-O, Caron E, Marin M-F, Chen J, Albouy G, Plante I, Sullivan MJ, Lupien SJ, Rainville P. The stress model of chronic pain: evidence from basal cortisol and hippocampal structure and function in humans. Brain 2013;136:815–27.
Verdejo-García A, López-Torrecillas F, Calandre EP, Delgado-Rodríguez A, Bechara A. Executive function and decision-making in women with fibromyalgia. Arch Clin Neuropsychol 2009;24:113–22.
Wang D-S, Tian Z, Guo Y-Y, Guo H-L, Kang W-B, Li S, Den Y-T, Li X-B, Feng B, Feng D, Zhao J-N, Liu G, Zhao M-G. Anxiolytic-like effects of translocator protein (TSPO) ligand ZBD-2 in an animal model of chronic pain. Mol Pain 2015;11:16.
Yue J, Wang X-S, Guo Y-Y, Zheng K-Y, Liu H-Y, Hu L-N, Zhao M-G, Liu S-B. Anxiolytic effect of CPEB1 knockdown on the amygdala of a mouse model of inflammatory pain. Brain Res Bull 2018;137:156–65.
Zheng J, Jiang Y-Y, Xu L-C, Ma L-Y, Liu F-Y, Cui S, Cai J, Liao F-F, Wan Y, Yi M. Adult hippocampal neurogenesis along the dorsoventral Axis contributes differentially to environmental enrichment combined with voluntary exercise in alleviating chronic inflammatory pain in mice. J Neurosci 2017;37:4145–57.
Zhong F, Liu L, Wei J-L, Hu Z-L, Li L, Wang S, Xu J-M, Zhou X-F, Li C-Q, Yang Z-Y, Dai R-P. Brain-Derived neurotrophic factor precursor in the Hippocampus regulates both depressive and anxiety-like behaviors in rats. Front Psychiatry 2018;9:776.