Structural and functional alterations in the retrosplenial cortex following neuropathic pain.
Journal
Pain
ISSN: 1872-6623
Titre abrégé: Pain
Pays: United States
ID NLM: 7508686
Informations de publication
Date de publication:
10 2019
10 2019
Historique:
pubmed:
31
5
2019
medline:
25
8
2020
entrez:
31
5
2019
Statut:
ppublish
Résumé
Human and animal imaging studies demonstrated that chronic pain profoundly alters the structure and the functionality of several brain regions. In this article, we conducted a longitudinal and multimodal study to assess how chronic pain affects the brain. Using the spared nerve injury model which promotes both long-lasting mechanical and thermal allodynia/hyperalgesia but also pain-associated comorbidities, we showed that neuropathic pain deeply modified the intrinsic organization of the brain functional network 1 and 2 months after injury. We found that both functional metrics and connectivity of the part A of the retrosplenial granular cortex (RSgA) were significantly correlated with the development of neuropathic pain behaviours. In addition, we found that the functional RSgA connectivity to the subiculum and the prelimbic system are significantly increased in spared nerve injury animals and correlated with peripheral pain thresholds. These brain regions were previously linked to the development of comorbidities associated with neuropathic pain. Using a voxel-based morphometry approach, we showed that neuropathic pain induced a significant increase of the gray matter concentration within the RSgA, associated with a significant activation of both astrocytes and microglial cells. Together, functional and morphological imaging metrics of the RSgA could be used as a predictive biomarker of neuropathic pain.
Identifiants
pubmed: 31145220
doi: 10.1097/j.pain.0000000000001610
pii: 00006396-201910000-00009
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2241-2254Références
Apkarian AV, Bushnell MC, Treede RD, Zubieta JK. Human brain mechanisms of pain perception and regulation in health and disease. Eur J Pain 2005;9:463–84.
Apkarian AV, Hashmi JA, Baliki MN. Pain and the brain: specificity and plasticity of the brain in clinical chronic pain. PAIN 2011;152:S49–64.
Apkarian AV, Mutso AA, Centeno MV, Kan L, Wu M, Levinstein M, Banisadr G, Gobeske KT, Miller RJ, Radulovic J, Hen R, Kessler JA. Role of adult hippocampal neurogenesis in persistent pain. PAIN 2016;157:418–28.
Arentsen T, Qian Y, Gkotzis S, Femenia T, Wang T, Udekwu K, Forssberg H, Diaz Heijtz R. The bacterial peptidoglycan-sensing molecule Pglyrp2 modulates brain development and behavior. Mol Psychiatry 2017;22:257–66.
Ashburner J. A fast diffeomorphic image registration algorithm. Neuroimage 2007;38:95–113.
Ashburner J, Friston KJ. Unified segmentation. Neuroimage 2005;26:839–51.
Ashburner J, Friston KJ. Voxel-based morphometry—the methods. Neuroimage 2000;11:805–21.
Baliki MN, Baria AT, Apkarian AV. The cortical rhythms of chronic back pain. J Neurosci 2011;31:13981–90.
Baliki MN, Chang PC, Baria AT, Centeno MV, Apkarian AV. Resting-sate functional reorganization of the rat limbic system following neuropathic injury. Sci Rep 2014;4:6186.
Becerra L, Bishop J, Barmettler G, Kainz V, Burstein R, Borsook D. Brain network alterations in the inflammatory soup animal model of migraine. Brain Res 2017;1660:36–46.
Bilbao A, Falfán-Melgoza C, Leixner S, Becker R, Singaravelu SK, Sack M, Sartorius A, Spanagel R, Weber-Fahr W. Longitudinal structural and functional brain network alterations in a mouse model of neuropathic pain. Neuroscience 2018;387:104–15.
Boly M, Faymonville ME, Schnakers C, Peigneux P, Lambermont B, Phillips C, Lancellotti P, Luxen A, Lamy M, Moonen G, Maquet P, Laureys S. Perception of pain in the minimally conscious state with PET activation: an observational study. Lancet Neurol 2008;7:1013–20.
Borsook D, Becerra L. CNS animal fMRI in pain and analgesia. Neurosci Biobehav Rev 2011;35:1125–43.
Borsook D, Becerra L, Hargreaves R. A role for fMRI in optimizing CNS drug development. Nat Rev Drug Discov 2006;5:411–24.
Choi Y, Yoon YW, Na HS, Kim SH, Chung JM. Behavioral signs of ongoing pain and cold allodynia in a rat model of neuropathic pain. PAIN 1994;59:369–76.
Colloca L, Ludman T, Bouhassira D, Baron R, Dickenson AH, Yarnitsky D, Freeman R, Truini A, Attal N, Finnerup NB, Eccleston C, Kalso E, Bennett DL, Dworkin RH, Raja SN. Neuropathic pain. Nat Rev Dis Primers 2017;3:17002.
Decosterd I, Woolf CJ. Spared nerve injury: an animal model of persistent peripheral neuropathic pain. PAIN 2000;87:149–58.
Dellu F, Mayo W, Cherkaoui J, Le Moal M, Simon H. A two-trial memory task with automated recording: study in young and aged rats. Brain Res 1992;588:132–9.
Flatters SJ, Bennett GJ. Studies of peripheral sensory nerves in paclitaxel-induced painful peripheral neuropathy: evidence for mitochondrial dysfunction. PAIN 2006;122:245–57.
Gosselin RD, Suter MR, Ji RR, Decosterd I. Glial cells and chronic pain. Neuroscientist 2010;16:519–31.
van Groen T, Wyss JM. Connections of the retrosplenial granular a cortex in the rat. J Comp Neurol 1990;300:593–606.
Hashmi JA, Kong J, Spaeth R, Khan S, Kaptchuk TJ, Gollub RL. Functional network architecture predicts psychologically mediated analgesia related to treatment in chronic knee pain patients. J Neurosci 2014;34:3924–36.
Henry DE, Chiodo AE, Yang W. Central nervous system reorganization in a variety of chronic pain states: a review. PM R 2011;3:1116–25.
Hubbard CS, Khan SA, Xu S, Cha M, Masri R, Seminowicz DA. Behavioral, metabolic and functional brain changes in a rat model of chronic neuropathic pain: a longitudinal MRI study. Neuroimage 2015;107:333–44.
Iannetti GD, Mouraux A. From the neuromatrix to the pain matrix (and back). Exp Brain Res 2010;205:1–12.
Jeong KY, Kang JH. Investigation of spinal nerve ligation-mediated functional activation of the rat brain using manganese-enhanced MRI. Exp Anim 2018;67:23–9.
Ji RR, Chamessian A, Zhang YQ. Pain regulation by non-neuronal cells and inflammation. Science 2016;354:572–7.
Keifer OP Jr, Hurt RC, Gutman DA, Keilholz SD, Gourley SL, Ressler KJ. Voxel-based morphometry predicts shifts in dendritic spine density and morphology with auditory fear conditioning. Nat Commun 2015;6:7582.
Kelly JR, Kennedy PJ, Cryan JF, Dinan TG, Clarke G, Hyland NP. Breaking down the barriers: the gut microbiome, intestinal permeability and stress-related psychiatric disorders. Front Cell Neurosci 2015;9:392.
Kelly RE, Alexopoulos GS, Wang Z, Gunning FM, Murphy CF, Morimoto SS, Kanellopoulos D, Jia Z, Lim KO, Hoptman MJ. Visual inspection of independent components: defining a procedure for artifact removal from fMRI data. J Neurosci Methods 2010;189:233–45.
Kucyi A, Davis KD. The dynamic pain connectome. Trends Neurosci 2015;38:86–95.
Kucyi A, Moayedi M, Weissman-Fogel I, Goldberg MB, Freeman BV, Tenenbaum HC, Davis KD. Enhanced medial prefrontal-default mode network functional connectivity in chronic pain and its association with pain rumination. J Neurosci 2014;34:3969–75.
Kunde V, Treede RD. Topography of middle-latency somatosensory evoked potentials following painful laser stimuli and non-painful electrical stimuli. Electroencephalogr Clin Neurophysiol 1993;88:280–9.
Kuzumaki N, Narita M, Narita M, Hareyama N, Niikura K, Nagumo Y, Nozaki H, Amano T, Suzuki T. Chronic pain-induced astrocyte activation in the cingulate cortex with no change in neural or glial differentiation from neural stem cells in mice. Neurosci Lett 2007;415:22–7.
Kwapis JL, Jarome TJ, Lee JL, Helmstetter FJ. The retrosplenial cortex is involved in the formation of memory for context and trace fear conditioning. Neurobiol Learn Mem 2015;123:110–16.
Leite-Almeida H, Almeida-Torres L, Mesquita AR, Pertovaara A, Sousa N, Cerqueira JJ, Almeida A. The impact of age on emotional and cognitive behaviours triggered by experimental neuropathy in rats. PAIN 2009;144:57–65.
Leite-Almeida H, Cerqueira JJ, Wei H, Ribeiro-Costa N, Anjos-Martins H, Sousa N, Pertovaara A, Almeida A. Differential effects of left/right neuropathy on rats' anxiety and cognitive behavior. PAIN 2012;153:2218–25.
Liang Z, King J, Zhang N. Intrinsic organization of the anesthetized brain. J Neurosci 2012;32:10183–91.
Liu X, Zhu XH, Zhang Y, Chen W. Neural origin of spontaneous hemodynamic fluctuations in rats under burst-suppression anesthesia condition. Cereb Cortex 2011;21:374–84.
Loggia ML, Kim J, Gollub RL, Vangel MG, Kirsch I, Kong J, Wasan AD, Napadow V. Default mode network connectivity encodes clinical pain: an arterial spin labeling study. PAIN 2013;154:24–33.
Lui F, Duzzi D, Corradini M, Serafini M, Baraldi P, Porro CA. Touch or pain? Spatio-temporal patterns of cortical fMRI activity following brief mechanical stimuli. PAIN 2008;138:362–74.
Magalhães R, Barrière DA, Novais A, Marques F, Marques P, Cerqueira J, Sousa JC, Cachia A, Boumezbeur F, Bottlaender M, Jay TM, Mériaux S, Sousa N. The dynamics of stress: a longitudinal MRI study of rat brain structure and connectome. Mol Psychiatry 2017;23:1998–2006.
Miller G. Neuroscience. Brain scans of pain raise questions for the law. Science 2009;323:195.
Mutso AA, Radzicki D, Baliki MN, Huang L, Banisadr G, Centeno MV, Radulovic J, Martina M, Miller RJ, Apkarian AV. Abnormalities in hippocampal functioning with persistent pain. J Neurosci 2012;32:5747–56.
Napadow V, Kim J, Clauw DJ, Harris RE. Decreased intrinsic brain connectivity is associated with reduced clinical pain in fibromyalgia. Arthritis Rheum 2012;64:2398–403.
Narita M, Kuzumaki N, Narita M, Kaneko C, Hareyama N, Miyatake M, Shindo K, Miyoshi K, Nakajima M, Nagumo Y, Sato F, Wachi H, Seyama Y, Suzuki T. Chronic pain-induced emotional dysfunction is associated with astrogliosis due to cortical delta-opioid receptor dysfunction. J Neurochem 2006;97:1369–78.
Paasonen J, Stenroos P, Salo RA, Kiviniemi V, Gröhn O. Functional connectivity under six anesthesia protocols and the awake condition in rat brain. Neuroimage 2018;172:9–20.
Papp EA, Leergaard TB, Calabrese E, Johnson GA, Bjaalie JG. Waxholm space atlas of the Sprague dawley rat brain. Neuroimage 2014;97:374–86.
Percie du Sert N, Rice ASC. Improving the translation of analgesic drugs to the clinic: animal models of neuropathic pain. Br J Pharmacol 2014;171:2951–63.
Perio A, Terranova JP, Worms P, Bluthe RM, Dantzer R, Biziere K. Specific modulation of social memory in rats by cholinomimetic and nootropic drugs, by benzodiazepine inverse agonists, but not by psychostimulants. Psychopharmacology (Berl) 1989;97:262–8.
Powell AL, Nelson AJD, Hindley E, Davies M, Aggleton JP, Vann SD. The rat retrosplenial cortex as a link for frontal functions: a lesion analysis. Behav Brain Res 2017;335:88–102.
Powell AL, Vann SD, Olarte-Sánchez CM, Kinnavane L, Davies M, Amin E, Aggleton JP, Nelson AJD. The retrosplenial cortex and object recency memory in the rat. Eur J Neurosci 2017;45:1451–64.
Reddan MC, Wager TD. Modeling pain using fMRI: from regions to biomarkers. Neurosci Bull 2018;34:208–15.
Reis GM, Dias QM, Silveira JWS, Del Vecchio F, Garcia-Cairasco N, Prado WA. Antinociceptive effect of stimulating the occipital or retrosplenial cortex in rats. J Pain 2010;11:1015–26.
Ren WJ, Liu Y, Zhou LJ, Li W, Zhong Y, Pang RP, Xin WJ, Wei XH, Wang J, Zhu HQ, Wu CY, Qin ZH, Liu G, Liu XG. Peripheral nerve injury leads to working memory deficits and dysfunction of the hippocampus by upregulation of TNF-α in rodents. Neuropsychopharmacology 2011;36:979–92.
Rossaneis AC, Reis GM, Prado WA. Stimulation of the occipital or retrosplenial cortex reduces incision pain in rats. Pharmacol Biochem Behav 2011;100:220–7.
Rubinov M, Sporns O. Complex network measures of brain connectivity: uses and interpretations. Neuroimage 2010;52:1059–69.
Salomons TV, Iannetti GD, Liang M, Wood JN. The “pain matrix” in pain-free individuals. JAMA Neurol 2016;73:755–6.
Salter MW, Stevens B. Microglia emerge as central players in brain disease. Nat Med 2017;23:1018–27.
Sawiak SJ, Picq JL, Dhenain M. Voxel-based morphometry analyses of in vivo MRI in the aging mouse lemur primate. Front Aging Neurosci 2014;6:82.
Sawiak SJ, Wood NI, Williams GB, Morton AJ, Carpenter TA. SPMMouse: a new toolbox for SPM in the animal brain. 17th Meeting of the Int'l Soc Mag Res in Med. Hawaii, USA 2009. p 1086.
Sawiak SJ, Wood NI, Williams GB, Morton AJ, Carpenter TA. Voxel-based morphometry with templates and validation in a mouse model of Huntington's disease. Magn Reson Imaging 2013;31:1522–31.
Schweinhardt P, Bountra C, Tracey I. Pharmacological FMRI in the development of new analgesic compounds. NMR Biomed 2006;19:702–11.
Seifert F, Jungfer I, Schmelz M, Maihöfner C. Representation of UV-B-induced thermal and mechanical hyperalgesia in the human brain: a functional MRI study. Hum Brain Mapp 2008;29:1327–42.
Seifert F, Maihöfner C. Representation of cold allodynia in the human brain—a functional MRI study. Neuroimage 2007;35:1168–80.
Seminowicz DA, Laferriere AL, Millecamps M, Yu JSC, Coderre TJ, Bushnell MC. MRI structural brain changes associated with sensory and emotional function in a rat model of long-term neuropathic pain. Neuroimage 2009;47:1007–14.
Sun YN, Luo JY, Rao ZR, Lan L, Duan L. GFAP and Fos immunoreactivity in lumbo-sacral spinal cord and medulla oblongata after chronic colonic inflammation in rats. World J Gastroenterol 2005;11:4827–32.
Todd TP, Bucci DJ. Retrosplenial cortex and long-term memory: molecules to behavior. Neural Plast 2015;2015:414173.
Valdes-Hernandez PA, Sumiyoshi A, Nonaka H, Haga R, Aubert-Vasquez E, Ogawa T, Iturria-Medina Y, Riera JJ, Kawashima R. An in vivo MRI template set for morphometry, tissue segmentation, and fMRI localization in rats. Front Neuroinform 2011;5:26.
Wager TD, Atlas LY, Lindquist MA, Roy M, Woo CW, Kross E. An fMRI-based neurologic signature of physical pain. N Engl J Med 2013;368:1388–97.
Whitfield-Gabrieli S, Nieto-Castanon A. Conn: a functional connectivity toolbox for correlated and anticorrelated brain networks. Brain Connect 2012;2:125–41.
Xia M, Wang J, He Y. BrainNet viewer: a network visualization tool for human brain connectomics. PLoS One 2013;8:e68910.
Zalesky A, Fornito A, Bullmore ET. Network-based statistic: identifying differences in brain networks. Neuroimage 2010;53:1197–207.
Zheng L, Cleppien D, Gass N, Falfan-Melgoza C, Vollmayr B, Hesser J, Weber-Fahr W, Sartorius A. Influence of regional cerebral blood volume on voxel-based morphometry. NMR Biomed 2016;29:787–95.
Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. PAIN 1983;16:109–10.