دورية أكاديمية
Chronic generalized pain disrupts whole brain functional connectivity in mice.
العنوان: | Chronic generalized pain disrupts whole brain functional connectivity in mice. |
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المؤلفون: | Nasseef MT; Douglas Hospital Research Center, Department of Psychiatry, School of Medicine, McGill University, Montreal, Quebec, Canada., Ma W; Douglas Hospital Research Center, Department of Psychiatry, School of Medicine, McGill University, Montreal, Quebec, Canada., Singh JP; Douglas Hospital Research Center, Department of Psychiatry, School of Medicine, McGill University, Montreal, Quebec, Canada., Dozono N; Department of Molecular Pharmacology, Kyoto University Graduate School of Pharmaceutical Sciences, Kyoto, 606-8501, Japan., Lançon K; Montreal Neurological institute, Department of Neurology & Neurosurgery, the Alan Edwards Centre for Research on Pain, Montreal Neurological Institute, Dept. Neurology & Neurosurgery, McGill University, Montreal, Quebec, Canada., Séguéla P; Montreal Neurological institute, Department of Neurology & Neurosurgery, the Alan Edwards Centre for Research on Pain, Montreal Neurological Institute, Dept. Neurology & Neurosurgery, McGill University, Montreal, Quebec, Canada., Darcq E; Douglas Hospital Research Center, Department of Psychiatry, School of Medicine, McGill University, Montreal, Quebec, Canada., Ueda H; Department of Molecular Pharmacology, Kyoto University Graduate School of Pharmaceutical Sciences, Kyoto, 606-8501, Japan., Kieffer BL; Douglas Hospital Research Center, Department of Psychiatry, School of Medicine, McGill University, Montreal, Quebec, Canada. brigitte.kieffer@douglas.mcgill.ca.; Douglas Hospital Research Center, Perry Pavilion Room E-3317.1, 6875 boulevard LaSalle, Montreal, Quebec, H4H 1R3, Canada. brigitte.kieffer@douglas.mcgill.ca. |
المصدر: | Brain imaging and behavior [Brain Imaging Behav] 2021 Oct; Vol. 15 (5), pp. 2406-2416. Date of Electronic Publication: 2021 Jan 11. |
نوع المنشور: | Journal Article |
اللغة: | English |
بيانات الدورية: | Publisher: Springer Country of Publication: United States NLM ID: 101300405 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1931-7565 (Electronic) Linking ISSN: 19317557 NLM ISO Abbreviation: Brain Imaging Behav Subsets: MEDLINE |
أسماء مطبوعة: | Original Publication: Secaucus, NJ : Springer |
مواضيع طبية MeSH: | Chronic Pain*/diagnostic imaging , Fibromyalgia*, Animals ; Brain/diagnostic imaging ; Brain Mapping ; Magnetic Resonance Imaging ; Mice ; Neural Pathways/diagnostic imaging |
مستخلص: | Fibromyalgia (FM) is a generalized chronic pain condition whose pathophysiology is poorly understood, and both basic and translational research are needed to advance the field. Here we used the Sluka model to test whether FM-like pain in mice would produce detectable brain modifications using resting-state (rs) functional Magnetic Resonance Imaging (fMRI). Mice received intramuscular acid saline treatment, images were acquired at 7 T 5 days post-treatment, and pain thresholds tested 3 weeks post-scanning. Data-driven Independent Component Analysis revealed significant reduction of functional connectivity (FC) across several component pairs, with major changes for the Retrosplenial cortex (RSP) central to the default mode network, and to a lesser extent the Periaqueductal gray (PAG), a key pain processing area. Seed-to-seed analysis focused on 14 pain-related areas showed strongest FC reduction for RSP with several cortical areas (somatosensory, prefrontal and insular), and for PAG with both cortical (somatosensory) and subcortical (habenula, thalamus, parabrachial nucleus) areas. RSP-PAG FC was also reduced, and this decreased FC tended to be positively correlated with pain levels at individual subject level. Finally, seed-voxelwise analysis focused on PAG confirmed seed-to-seed findings and, also detected reduced PAG FC with the anterior cingulate cortex, increasingly studied in aversive pain effects. In conclusion, FM-like pain triggers FC alterations in the mouse, which are detected by rs-fMRI and are reminiscent of some human findings. The study reveals the causal fingerprint of FM-like pain in rodents, and indicates that both RSP and PAG connectional patterns could be suitable biomarkers, with mechanistic and translational value, for further investigations. (© 2021. The Author(s), under exclusive licence to Springer Science+Business Media, LLC part of Springer Nature.) |
References: | Aimone, L. D., & Gebhart, G. F. (1987). Spinal monoamine mediation of stimulation-produced antinociception from the lateral hypothalamus. Brain Research, 403, 290–300. (PMID: 288160710.1016/0006-8993(87)90066-72881607) Barriere, D. A., Hamieh, A. M., Magalhaes, R., Traore, A., Barbier, J., et al. (2019). Structural and functional alterations in the retrosplenial cortex following neuropathic pain. Pain, 160, 2241–2254. (PMID: 3114522010.1097/j.pain.000000000000161031145220) Basbaum, A. I., Bautista, D. M., Scherrer, G., & Julius, D. (2009). Cellular and molecular mechanisms of pain. Cell, 139, 267–284. (PMID: 19837031285264310.1016/j.cell.2009.09.028) Ben Hamida, S., Mendonca-Netto, S., Arefin, T. M., Nasseef, M. T., Boulos, L. J., et al. (2018). Increased alcohol seeking in mice lacking Gpr88 involves dysfunctional Mesocorticolimbic networks. Biological Psychiatry, 84, 202–212. (PMID: 29580570605457110.1016/j.biopsych.2018.01.026) Benlidayi, I. C. (2019). Role of inflammation in the pathogenesis and treatment of fibromyalgia. Rheumatology International, 39, 781–791. (PMID: 10.1007/s00296-019-04251-6) Bliss, T. V., Collingridge, G. L., Kaang, B. K., & Zhuo, M. (2016). Synaptic plasticity in the anterior cingulate cortex in acute and chronic pain. Nature Reviews. Neuroscience, 17, 485–496. (PMID: 2730711810.1038/nrn.2016.6827307118) Borsook, D., Linnman, C., Faria, V., Strassman, A. M., Becerra, L., & Elman, I. (2016). Reward deficiency and anti-reward in pain chronification. Neuroscience and Biobehavioral Reviews, 68, 282–297. (PMID: 2724651910.1016/j.neubiorev.2016.05.03327246519) Boulos, L. J., Darcq, E., & Kieffer, B. L. (2017). Translating the Habenula-from rodents to humans. Biological Psychiatry, 81, 296–305. (PMID: 2752782210.1016/j.biopsych.2016.06.00327527822) Boulos, L. J., Nasseef, M. T., McNicholas, M., Mechling, A., Harsan, L. A., Darcq, E., Ben Hamida, S., & Kieffer, B. L. (2019). TouchScreen-based phenotyping: Altered stimulus/reward association and lower perseveration to gain a reward in mu opioid receptor knockout mice. Scientific Reports, 9, 4044. (PMID: 30858487641172910.1038/s41598-019-40622-6) Broyd, S. J., Demanuele, C., Debener, S., Helps, S. K., James, C. J., & Sonuga-Barke, E. J. (2009). Default-mode brain dysfunction in mental disorders: A systematic review. Neuroscience and Biobehavioral Reviews, 33, 279–296. (PMID: 1882419510.1016/j.neubiorev.2008.09.00218824195) Cagnie, B., Coppieters, I., Denecker, S., Six, J., Danneels, L., & Meeus, M. (2014). Central sensitization in fibromyalgia? A systematic review on structural and functional brain MRI. Seminars in Arthritis and Rheumatism, 44, 68–75. (PMID: 2450840610.1016/j.semarthrit.2014.01.00124508406) Charbogne, P., Gardon, O., Martin-Garcia, E., Keyworth, H. L., Matsui, A., et al. (2017). Mu opioid receptors in gamma-Aminobutyric Acidergic forebrain neurons moderate motivation for heroin and palatable food. Biological Psychiatry, 81, 778–788. (PMID: 2818564510.1016/j.biopsych.2016.12.02228185645) Cifre, I., Sitges, C., Fraiman, D., Munoz, M. A., Balenzuela, P., et al. (2012). Disrupted functional connectivity of the pain network in fibromyalgia. Psychosomatic Medicine, 74, 55–62. (PMID: 2221024210.1097/PSY.0b013e3182408f0422210242) Clauw, D. J. (2014). Fibromyalgia: a clinical review. JAMA, 311, 1547–1555. (PMID: 2473736710.1001/jama.2014.326624737367) Coulombe, M. A., Lawrence, K. S., Moulin, D. E., Morley-Forster, P., Shokouhi, M., Nielson, W. R., & Davis, K. D. (2017). Lower functional connectivity of the periaqueductal gray is related to negative affect and clinical manifestations of fibromyalgia. Frontiers in Neuroanatomy, 11, 47. (PMID: 28642688546292610.3389/fnana.2017.00047) de Oliveira, R., de Oliveira, R. C., Falconi-Sobrinho, L. L., da Silva, S. R., & Jr., Coimbra NC. (2017). 5-Hydroxytryptamine2A/2C receptors of nucleus raphe magnus and gigantocellularis/paragigantocellularis pars alpha reticular nuclei modulate the unconditioned fear-induced antinociception evoked by electrical stimulation of deep layers of the superior colliculus and dorsal periaqueductal grey matter. Behavioural Brain Research, 316, 294–304. (PMID: 2761634410.1016/j.bbr.2016.09.01627616344) DeSantana, J. M., da Cruz, K. M., & Sluka, K. A. (2013). Animal models of fibromyalgia. Arthritis Research & Therapy, 15, 222. (PMID: 10.1186/ar4402) Fakhoury, M. (2017). The habenula in psychiatric disorders: More than three decades of translational investigation. Neuroscience and Biobehavioral Reviews, 83, 721–735. (PMID: 2822309610.1016/j.neubiorev.2017.02.010) Fayyaz, A., Ghanim, U., & Sung-Ho, K. (2012). A neighborhood method for statistical analysis of fMRI data. Open Journal of Biophysics, 2012. Greicius, M. D., Krasnow, B., Reiss, A. L., & Menon, V. (2003). Functional connectivity in the resting brain: A network analysis of the default mode hypothesis. Proceedings of the National Academy of Sciences of the United States of America, 100, 253–258. (PMID: 1250619410.1073/pnas.0135058100) Häuser, W., Clauw, D., & Fitzcharles, M.-A. (2019). Fibromyalgia as a chronic primary pain syndrome: Issues to discuss. Pain, 160, 2651–2652. (PMID: 3162607410.1097/j.pain.000000000000168631626074) Juarez-Salinas, D. L., Braz, J. M., Etlin, A., Gee, S., Sohal, V., & Basbaum, A. I. (2019). GABAergic cell transplants in the anterior cingulate cortex reduce neuropathic pain aversiveness. Brain, 142, 2655–2669. (PMID: 31321411675216810.1093/brain/awz203) Kim J, Loggia ML, Cahalan CM, Harris RE, Beissner FDPN, et al. 2015. The somatosensory link in fibromyalgia: Functional connectivity of the primary somatosensory cortex is altered by sustained pain and is associated with clinical/autonomic dysfunction. Arthritis & rheumatology (Hoboken, N.J.) 67: 1395-405. Kucyi, A., & Davis, K. D. (2015). The dynamic pain connectome. Trends in Neurosciences, 38, 86–95. (PMID: 2554128710.1016/j.tins.2014.11.006) Lee J, Protsenko E, Lazaridou A, Franceschelli O, Ellingsen DM, et al. 2018. Encoding of self-referential pain Catastrophizing in the posterior cingulate cortex in fibromyalgia. Arthritis & rheumatology (Hoboken, N.J.), 70: 1308-18. Littlejohn G, Guymer E. (2018) Seminars in immunopathology, 40: 291-300. Springer. Ma W, St-Jacques B, Rudakou U, Kim YN. 2017. Stimulating TRPV1 externalization and synthesis in dorsal root ganglion neurons contributes to PGE2 potentiation of TRPV1 activity and nociceptor sensitization. European journal of pain (London, England), 21: 575-93. McBeth, J., & Mulvey, M. R. (2012). Fibromyalgia: Mechanisms and potential impact of the ACR 2010 classification criteria. Nature Reviews Rheumatology, 8, 108–116. (PMID: 2227007710.1038/nrrheum.2011.21622270077) Mechling, A. E., Arefin, T., Lee, H. L., Bienert, T., Reisert, M., Ben Hamida, S., Darcq, E., Ehrlich, A., Gaveriaux-Ruff, C., Parent, M. J., Rosa-Neto, P., Hennig, J., von Elverfeldt, D., Kieffer, B. L., & Harsan, L. A. (2016). Deletion of the mu opioid receptor gene in mice reshapes the reward-aversion connectome. Proceedings of the National Academy of Sciences of the United States of America, 113, 11603–11608. (PMID: 27671662506832410.1073/pnas.1601640113) Metyas, S., Rezk, T., Arkfeld, D., & Leptich, T. (2017). Autoinflammation and immunomodulation in inflammatory fibromyalgia syndrome-a review. Current Rheumatology Reviews, 13, 98–102. (PMID: 2765562627655626) Nagakura, Y. (2015). Recent advancements in animal models of fibromyalgia. MYOPAIN, 23, 104–111. (PMID: 10.1080/24708593.2016.1273986) Nasseef, M. T. (2015). Measuring directed functional connectivity in mouse fMRI networks using granger causality. University of Trento. Nasseef, M. T., Devenyi, G. A., Mechling, A. E., Harsan, L. A., Chakravarty, M. M., Kieffer, B. L., & Darcq, E. (2018). Deformation-based Morphometry MRI reveals brain structural modifications in living mu opioid receptor knockout mice. Frontiers in Psychiatry, 9, 643. (PMID: 30559685628711310.3389/fpsyt.2018.00643) Nasseef, M. T., Singh, J. P., Ehrlich, A. T., McNicholas, M., Park, D. W., Ma, W., Kulkarni, P., Kieffer, B. L., & Darcq, E. (2019). Oxycodone-mediated activation of the mu opioid receptor reduces whole brain functional connectivity in mice. ACS Pharmacology & Translational Science, 2, 264–274. (PMID: 10.1021/acsptsci.9b00021) Nishiyori, M., Nagai, J., Nakazawa, T., & Ueda, H. (2010). Absence of morphine analgesia and its underlying descending serotonergic activation in an experimental mouse model of fibromyalgia. Neuroscience Letters, 472, 184–187. (PMID: 2013897010.1016/j.neulet.2010.01.08020138970) Raichle, M. E., MacLeod, A. M., Snyder, A. Z., Powers, W. J., Gusnard, D. A., & Shulman, G. L. (2001). A default mode of brain function. Proceedings of the National Academy of Sciences of the United States of America, 98, 676–682. (PMID: 112090641464710.1073/pnas.98.2.676) Ramírez-Tejero, J. A., Martínez-Lara, E., Rus, A., Camacho, M. V., Del Moral, M. L., & Siles, E. (2018). Insight into the biological pathways underlying fibromyalgia by a proteomic approach. Journal of Proteomics, 186, 47–55. (PMID: 3003016310.1016/j.jprot.2018.07.00930030163) Reichling, D. B., Kwiat, G. C., & Basbaum, A. I. (1988). Anatomy, physiology and pharmacology of the periaqueductal gray contribution to antinociceptive controls. Progress in Brain Research, 77, 31–46. (PMID: 306417310.1016/S0079-6123(08)62777-63064173) Roeder, Z., Chen, Q., Davis, S., Carlson, J. D., Tupone, D., & Heinricher, M. M. (2016). Parabrachial complex links pain transmission to descending pain modulation. Pain, 157, 2697–2708. (PMID: 27657698511373910.1097/j.pain.0000000000000688) Sarzi-Puttini, P., Atzeni, F., Masala, I. F., Salaffi, F., Chapman, J., & Choy, E. (2018). Are the ACR 2010 diagnostic criteria for fibromyalgia better than the 1990 criteria? Autoimmunity Reviews, 17, 33–35. (PMID: 2910883110.1016/j.autrev.2017.11.00729108831) Sawaddiruk, P., Paiboonworachat, S., Chattipakorn, N., & Chattipakorn, S. C. (2017). Alterations of brain activity in fibromyalgia patients. Journal of clinical neuroscience : official journal of the Neurosurgical Society of Australasia, 38, 13–22. (PMID: 10.1016/j.jocn.2016.12.014) Sforazzini, F., Schwarz, A. J., Galbusera, A., Bifone, A., & Gozzi, A. (2014). Distributed BOLD and CBV-weighted resting-state networks in the mouse brain. NeuroImage, 87, 403–415. (PMID: 2408050410.1016/j.neuroimage.2013.09.05024080504) Shelton, L., Becerra, L., & Borsook, D. (2012a). Unmasking the mysteries of the habenula in pain and analgesia. Progress in Neurobiology, 96, 208–219. (PMID: 22270045346572210.1016/j.pneurobio.2012.01.004) Shelton, L., Pendse, G., Maleki, N., Moulton, E. A., Lebel, A., Becerra, L., & Borsook, D. (2012b). Mapping pain activation and connectivity of the human habenula. Journal of Neurophysiology, 107, 2633–2648. (PMID: 22323632336227710.1152/jn.00012.2012) Sluka, K. A., & Clauw, D. J. (2016). Neurobiology of fibromyalgia and chronic widespread pain. Neuroscience, 338, 114–129. (PMID: 2729164110.1016/j.neuroscience.2016.06.00627291641) Sluka, K. A., Kalra, A., & Moore, S. A. (2001). Unilateral intramuscular injections of acidic saline produce a bilateral, long-lasting hyperalgesia. Muscle & Nerve, 24, 37–46. (PMID: 10.1002/1097-4598(200101)24:1<37::AID-MUS4>3.0.CO;2-8) Sluka, K. A., Rohlwing, J., Bussey, R., Eikenberry, S., & Wilken, J. (2002). Chronic muscle pain induced by repeated acid injection is reversed by spinally administered μ-and δ-, but not κ-, opioid receptor agonists. Journal of Pharmacology and Experimental Therapeutics, 302, 1146–1150. (PMID: 10.1124/jpet.102.033167) Stafford, J. M., Jarrett, B. R., Miranda-Dominguez, O., Mills, B. D., Cain, N., Mihalas, S., Lahvis, G. P., Lattal, K. M., Mitchell, S. H., David, S. V., Fryer, J. D., Nigg, J. T., & Fair, D. A. (2014). Large-scale topology and the default mode network in the mouse connectome. Proceedings of the National Academy of Sciences of the United States of America, 111, 18745–18750. (PMID: 25512496428453510.1073/pnas.1404346111) Truini, A., Tinelli, E., Gerardi, M. C., Calistri, V., Iannuccelli, C., la Cesa, S., Tarsitani, L., Mainero, C., Sarzi-Puttini, P., Cruccu, G., Caramia, F., & di Franco, M. (2016). Abnormal resting state functional connectivity of the periaqueductal grey in patients with fibromyalgia. Clinical and Experimental Rheumatology, 34, S129–S133. (PMID: 2715739727157397) Ueda H, Neyama H. 2017. LPA1 receptor involvement in fibromyalgia-like pain induced by intermittent psychological stress, empathy. Neurobiology of pain (Cambridge, Mass.), 1: 16-25. Vincent, J. L., Patel, G. H., Fox, M. D., Snyder, A. Z., Baker, J. T., van Essen, D. C., Zempel, J. M., Snyder, L. H., Corbetta, M., & Raichle, M. E. (2007). Intrinsic functional architecture in the anaesthetized monkey brain. Nature, 447, 83–86. (PMID: 1747626710.1038/nature0575817476267) |
معلومات مُعتمدة: | P50 DA005010 United States DA NIDA NIH HHS; U01 AA016658 United States AA NIAAA NIH HHS; 16658 United States AA NIAAA NIH HHS; 05010 United States DA NIDA NIH HHS; 05010 United States DA NIDA NIH HHS; 16658 United States AA NIAAA NIH HHS |
فهرسة مساهمة: | Keywords: Biomarker; Fibromyalgia; Mice; Periaqueductal gray; Resting-state fMRI; Retrosplenial cortex; Sluka model |
تواريخ الأحداث: | Date Created: 20210111 Date Completed: 20211012 Latest Revision: 20211014 |
رمز التحديث: | 20221213 |
مُعرف محوري في PubMed: | PMC8272737 |
DOI: | 10.1007/s11682-020-00438-9 |
PMID: | 33428113 |
قاعدة البيانات: | MEDLINE |
تدمد: | 1931-7565 |
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DOI: | 10.1007/s11682-020-00438-9 |