Transcranial Direct Current Stimulation Alleviates the Chronic Pain of Osteoarthritis by Modulating NMDA Receptors in Midbrain Periaqueductal Gray in Rats

References

• Poulet B, Staines KA. New developments in osteoarthritis and cartilage biology. Curr Opin Pharmacol. 2016;28:8–13. doi:10.1016/j.coph.2016.02.009
   PubMed Web of Science ®Google Scholar
• Schaible HG. Mechanisms of chronic pain in osteoarthritis. Curr Rheumatol Rep. 2012;14(6):549–556. doi:10.1007/s11926-012-0279-x
   PubMed Web of Science ®Google Scholar
• Woolf CJ. Central sensitization: uncovering the relation between pain and plasticity. Anesthesiology. 2007;106(4):864–867. doi:10.1097/01.anes.0000264769.87038.55
   PubMed Web of Science ®Google Scholar
• Hochberg MC, Altman RD, April KT, et al. American College of Rheumatology 2012 recommendations for the use of nonpharmacologic and pharmacologic therapies in osteoarthritis of the hand, hip, and knee. Arthritis Care Res. 2012;64(4):465–474. doi:10.1002/acr.21596
   PubMed Web of Science ®Google Scholar
• Tavares D, Okazaki J, Rocha AP, et al. Effects of transcranial direct current stimulation on knee osteoarthritis pain in elderly subjects with defective endogenous pain-inhibitory systems: protocol for a randomized controlled trial. JMIR Res Protoc. 2018;7(10):e11660. doi:10.2196/11660
   PubMedGoogle Scholar
• Hawker GA. Who, when, and why total joint replacement surgery? The patient’s perspective. Curr Opin Rheumatol. 2006;18(5):526–530. doi:10.1097/01.bor.0000240367.62583.51
   PubMed Web of Science ®Google Scholar
• Bourne RB, Chesworth BM, Davis AM, Mahomed NN, Charron KD. Patient satisfaction after total knee arthroplasty: who is satisfied and who is not? Clin Orthop Relat Res. 2010;468(1):57–63. doi:10.1007/s11999-009-1119-9
   PubMed Web of Science ®Google Scholar
• Kwon M, Altin M, Duenas H, Alev L. The role of descending inhibitory pathways on chronic pain modulation and clinical implications. Pain Pract. 2014;14(7):656–667. doi:10.1111/papr.12145
   PubMed Web of Science ®Google Scholar
• Finnerup NB, Sindrup SH, Jensen TS. Chronic neuropathic pain: mechanisms, drug targets and measurement. Fundam Clin Pharmacol. 2007;21(2):129–136. doi:10.1111/j.1472-8206.2007.00474.x
   PubMed Web of Science ®Google Scholar
• Staud R. Evidence for shared pain mechanisms in osteoarthritis, low back pain, and fibromyalgia. Curr Rheumatol Rep. 2011;13(6):513–520. doi:10.1007/s11926-011-0206-6
   PubMed Web of Science ®Google Scholar
• Porreca F, Ossipov MH, Gebhart GF. Chronic pain and medullary descending facilitation. Trends Neurosci. 2002;25(6):319–325. doi:10.1016/S0166-2236(02)02157-4
   PubMed Web of Science ®Google Scholar
• Fields HL, Malick A, Burstein R. Dorsal horn projection targets of ON and OFF cells in the rostral ventromedial medulla. J Neurophysiol. 1995;74(4):1742–1759. doi:10.1152/jn.1995.74.4.1742
   PubMed Web of Science ®Google Scholar
• Mantyh PW. Connections of midbrain periaqueductal gray in the monkey. II. Descending efferent projections. J Neurophysiol. 1983;49(3):582–594. doi:10.1152/jn.1983.49.3.582
   PubMed Web of Science ®Google Scholar
• Beitz AJ. The sites of origin brain stem neurotensin and serotonin projections to the rodent nucleus raphe magnus. J Neurosci. 1982;2(7):829–842. doi:10.1523/JNEUROSCI.02-07-00829.1982
   PubMed Web of Science ®Google Scholar
• Jensen TS, Yaksh TL. The antinociceptive activity of excitatory amino acids in the rat brainstem: an anatomical and pharmacological analysis. Brain Res. 1992;569(2):255–267. doi:10.1016/0006-8993(92)90637-O
   PubMed Web of Science ®Google Scholar
• Davies SN, Lodge D. Evidence for involvement of N-methylaspartate receptors in ‘wind-up’ of class 2 neurones in the dorsal horn of the rat. Brain Res. 1987;424(2):402–406. doi:10.1016/0006-8993(87)91487-9
   PubMed Web of Science ®Google Scholar
• Dickenson AH, Sullivan AF. Evidence for a role of the NMDA receptor in the frequency dependent potentiation of deep rat dorsal horn nociceptive neurones following C fibre stimulation. Neuropharmacology. 1987;26(8):1235–1238. doi:10.1016/0028-3908(87)90275-9
   PubMed Web of Science ®Google Scholar
• Hu J, Wang Z, Guo YY, et al. A role of periaqueductal grey NR2B-containing NMDA receptor in mediating persistent inflammatory pain. Mol Pain. 2009;5:71. doi:10.1186/1744-8069-5-71
   PubMed Web of Science ®Google Scholar
• Zhuo M. Glutamate receptors and persistent pain: targeting forebrain NR2B subunits. Drug Discov Today. 2002;7(4):259–267. doi:10.1016/S1359-6446(01)02138-9
   PubMed Web of Science ®Google Scholar
• Gogas KR. Glutamate-based therapeutic approaches: NR2B receptor antagonists. Curr Opin Pharmacol. 2006;6(1):68–74. doi:10.1016/j.coph.2005.11.001
   PubMed Web of Science ®Google Scholar
• Nakazato E, Kato A, Watanabe S. Brain but not spinal NR2B receptor is responsible for the anti-allodynic effect of an NR2B subunit-selective antagonist CP-101,606 in a rat chronic constriction injury model. Pharmacology. 2005;73(1):8–14. doi:10.1159/000081069
   PubMed Web of Science ®Google Scholar
• Harris JA. Using c-fos as a neural marker of pain. Brain Res Bull. 1998;45(1):1–8. doi:10.1016/S0361-9230(97)00277-3
   PubMed Web of Science ®Google Scholar
• Coggeshall RE. Fos, nociception and the dorsal horn. Prog Neurobiol. 2005;77(5):299–352. doi:10.1016/j.pneurobio.2005.11.002
   PubMed Web of Science ®Google Scholar
• Miranda PC, Lomarev M, Hallett M. Modeling the current distribution during transcranial direct current stimulation. Clin Neurophysiol. 2006;117(7):1623–1629. doi:10.1016/j.clinph.2006.04.009
   PubMed Web of Science ®Google Scholar
• Wagner T, Valero-Cabre A, Pascual-Leone A. Noninvasive human brain stimulation. Annu Rev Biomed Eng. 2007;9(1):527–565. doi:10.1146/annurev.bioeng.9.061206.133100
   PubMed Web of Science ®Google Scholar
• Nitsche MA, Paulus W. Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J Physiol. 2000;527(Pt 3):633–639. doi:10.1111/j.1469-7793.2000.t01-1-00633.x
   PubMed Web of Science ®Google Scholar
• Nitsche MA, Fricke K, Henschke U, et al. Pharmacological modulation of cortical excitability shifts induced by transcranial direct current stimulation in humans. J Physiol. 2003;553(Pt 1):293–301. doi:10.1113/jphysiol.2003.049916
   PubMed Web of Science ®Google Scholar
• Artola A, Brocher S, Singer W. Different voltage-dependent thresholds for inducing long-term depression and long-term potentiation in slices of rat visual cortex. Nature. 1990;347(6288):69–72. doi:10.1038/347069a0
   PubMed Web of Science ®Google Scholar
• Liebetanz D, Nitsche MA, Tergau F, Paulus W. Pharmacological approach to the mechanisms of transcranial DC-stimulation-induced after-effects of human motor cortex excitability. Brain. 2002;125(Pt 10):2238–2247. doi:10.1093/brain/awf238
   PubMed Web of Science ®Google Scholar
• Laste G, Caumo W, Adachi LN, et al. After-effects of consecutive sessions of transcranial direct current stimulation (tDCS) in a rat model of chronic inflammation. Exp Brain Res. 2012;221(1):75–83. doi:10.1007/s00221-012-3149-x
   PubMed Web of Science ®Google Scholar
• Roizenblatt S, Fregni F, Gimenez R, et al. Site-specific effects of transcranial direct current stimulation on sleep and pain in fibromyalgia: a randomized, sham-controlled study. Pain Pract. 2007;7(4):297–306. doi:10.1111/j.1533-2500.2007.00152.x
   PubMedGoogle Scholar
• Fregni F, Boggio PS, Lima MC, et al. A sham-controlled, Phase II trial of transcranial direct current stimulation for the treatment of central pain in traumatic spinal cord injury. Pain. 2006;122(1–2):197–209. doi:10.1016/j.pain.2006.02.023
   PubMed Web of Science ®Google Scholar
• Ahn H, Woods AJ, Kunik ME, et al. Efficacy of transcranial direct current stimulation over primary motor cortex (anode) and contralateral supraorbital area (cathode) on clinical pain severity and mobility performance in persons with knee osteoarthritis: an experimenter- and participant-blinded, randomized, sham-controlled pilot clinical study. Brain Stimul. 2017;10(5):902–909. doi:10.1016/j.brs.2017.05.007
   PubMed Web of Science ®Google Scholar
• Sajadi S, Karimi M, Forogh B, Raissi GR, Zarnegar F, Ahadi T. Randomized clinical trial comparing of transcranial direct current stimulation (tDCS) and transcutaneous electrical nerve stimulation (TENS) in knee osteoarthritis. Neurophysiol Clin. 2020;50(5):367–374. doi:10.1016/j.neucli.2020.08.005
   PubMed Web of Science ®Google Scholar
• Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain. 1983;16(2):109–110. doi:10.1016/0304-3959(83)90201-4
   PubMed Web of Science ®Google Scholar
• Havelin J, Imbert I, Cormier J, Allen J, Porreca F, King T. Central sensitization and neuropathic features of ongoing pain in a rat model of advanced osteoarthritis. J Pain. 2016;17(3):374–382. doi:10.1016/j.jpain.2015.12.001
   PubMed Web of Science ®Google Scholar
• Watson C, Paxinos G. The Rat Brain in Stereotaxic Coordinates. 6th ed. Amsterdam: Academic Press/Elsevier; 2007.
   Google Scholar
• Spezia AL, Quevedo AS, de Souza A, et al. Exogenously induced brain activation regulates neuronal activity by top-down modulation: conceptualized model for electrical brain stimulation. Exp Brain Res. 2015;233(5):1377–1389. doi:10.1007/s00221-015-4212-1
   PubMed Web of Science ®Google Scholar
• Leffa DT, Bellaver B, Salvi AA, et al. Transcranial direct current stimulation improves long-term memory deficits in an animal model of attention-deficit/hyperactivity disorder and modulates oxidative and inflammatory parameters. Brain Stimul. 2018;11(4):743–751. doi:10.1016/j.brs.2018.04.001
   PubMed Web of Science ®Google Scholar
• Lopes BC, Medeiros LF, Silva DSV, et al. Transcranial direct current stimulation combined with exercise modulates the inflammatory profile and hyperalgesic response in rats subjected to a neuropathic pain model: long-term effects. Brain Stimul. 2020;13(3):774–782. doi:10.1016/j.brs.2020.02.025
   PubMed Web of Science ®Google Scholar
• Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL. Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods. 1994;53(1):55–63. doi:10.1016/0165-0270(94)90144-9
   PubMed Web of Science ®Google Scholar
• Netto CA, Siegfried B, Izquierdo I. Analgesia induced by exposure to a novel environment in rats: effect of concurrent and post-training stressful stimulation. Behav Neural Biol. 1987;48(2):304–309. doi:10.1016/S0163-1047(87)90850-8
   PubMedGoogle Scholar
• Hargreaves K, Dubner R, Brown F, Flores C, Joris J. A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain. 1988;32(1):77–88. doi:10.1016/0304-3959(88)90026-7
   PubMed Web of Science ®Google Scholar
• Okun A, Liu P, Davis P, et al. Afferent drive elicits ongoing pain in a model of advanced osteoarthritis. Pain. 2012;153(4):924–933. doi:10.1016/j.pain.2012.01.022
   PubMed Web of Science ®Google Scholar
• Millan MJ. The induction of pain: an integrative review. Prog Neurobiol. 1999;57(1):1–164. doi:10.1016/s0301-0082(98)00048-3
   PubMed Web of Science ®Google Scholar
• Reidler JS, Mendonca ME, Santana MB, et al. Effects of motor cortex modulation and descending inhibitory systems on pain thresholds in healthy subjects. J Pain. 2012;13(5):450–458. doi:10.1016/j.jpain.2012.01.005
   PubMed Web of Science ®Google Scholar
• Drouot X, Nguyen JP, Peschanski M, Lefaucheur JP. The antalgic efficacy of chronic motor cortex stimulation is related to sensory changes in the painful zone. Brain. 2002;125(Pt 7):1660–1664. doi:10.1093/brain/awf161
   PubMed Web of Science ®Google Scholar
• Lefaucheur JP. The use of repetitive transcranial magnetic stimulation (rTMS) in chronic neuropathic pain. Neurophysiol Clin. 2006;36(3):117–124. doi:10.1016/j.neucli.2006.08.002
   PubMed Web of Science ®Google Scholar
• Fregni F, Pascual-Leone A, Freedman SD. Pain in chronic pancreatitis: a salutogenic mechanism or a maladaptive brain response? Pancreatology. 2007;7(5–6):411–422. doi:10.1159/000108958
   PubMed Web of Science ®Google Scholar
• Nguyen JP, Nizard J, Keravel Y, Lefaucheur JP. Invasive brain stimulation for the treatment of neuropathic pain. Nat Rev Neurol. 2011;7(12):699–709. doi:10.1038/nrneurol.2011.138
   PubMed Web of Science ®Google Scholar
• Lima MC, Fregni F. Motor cortex stimulation for chronic pain: systematic review and meta-analysis of the literature. Neurology. 2008;70(24):2329–2337. doi:10.1212/01.wnl.0000314649.38527.93
   PubMed Web of Science ®Google Scholar
• Bandler R, Shipley MT. Columnar organization in the midbrain periaqueductal gray: modules for emotional expression? Trends Neurosci. 1994;17(9):379–389. doi:10.1016/0166-2236(94)90047-7
   PubMed Web of Science ®Google Scholar
• Noh A, Ismail C. A review on chronic pain in rheumatoid arthritis: a focus on activation of NR2B subunit of N-Methyl-D-Aspartate receptors. Malays J Med Sci. 2020;27(1):6–21. doi:10.21315/mjms2020.27.1.2
   PubMed Web of Science ®Google Scholar
• Sandkuhler J, Fu QG, Zimmermann M. Spinal pathways mediating tonic or stimulation-produced descending inhibition from the periaqueductal gray or nucleus raphe magnus are separate in the cat. J Neurophysiol. 1987;58(2):327–341. doi:10.1152/jn.1987.58.2.327
   PubMed Web of Science ®Google Scholar
• Paxinos G. The Rat Nervous System. 2nd ed. San Diego: Academic Press; 1995.
   Google Scholar
• Wu LJ, Zhuo M. Targeting the NMDA receptor subunit NR2B for the treatment of neuropathic pain. Neurotherapeutics. 2009;6(4):693–702. doi:10.1016/j.nurt.2009.07.008
   PubMed Web of Science ®Google Scholar
• Ramos CM, Da SL, Menescal-de-oliveira L. Modulation of tonic immobility in Guinea pig PAG by homocysteic acid, a glutamate agonist. Physiol Behav. 2008;94(3):468–473. doi:10.1016/j.physbeh.2008.02.013
   PubMed Web of Science ®Google Scholar
• Berrino L, Oliva P, Rossi F, Palazzo E, Nobili B, Maione S. Interaction between metabotropic and NMDA glutamate receptors in the periaqueductal grey pain modulatory system. Naunyn Schmiedebergs Arch Pharmacol. 2001;364(5):437–443. doi:10.1007/s002100100477
   PubMed Web of Science ®Google Scholar
• Palazzo E, Marabese I, de Novellis V, et al. Metabotropic and NMDA glutamate receptors participate in the cannabinoid-induced antinociception. Neuropharmacology. 2001;40(3):319–326. doi:10.1016/S0028-3908(00)00160-X
   PubMed Web of Science ®Google Scholar
• Narita M, Ozaki S, Narita M, Ise Y, Yajima Y, Suzuki T. Change in the expression of c-fos in the rat brain following sciatic nerve ligation. Neurosci Lett. 2003;352(3):231–233. doi:10.1016/j.neulet.2003.08.052
   PubMed Web of Science ®Google Scholar
• Takeda R, Watanabe Y, Ikeda T, et al. Analgesic effect of milnacipran is associated with c-Fos expression in the anterior cingulate cortex in the rat neuropathic pain model. Neurosci Res. 2009;64(4):380–384. doi:10.1016/j.neures.2009.04.010
   PubMed Web of Science ®Google Scholar
• Fertonani A, Rosini S, Cotelli M, Rossini PM, Miniussi C. Naming facilitation induced by transcranial direct current stimulation. Behav Brain Res. 2010;208(2):311–318. doi:10.1016/j.bbr.2009.10.030
   PubMed Web of Science ®Google Scholar
• Krause B, Marquez-Ruiz J, Cohen KR. The effect of transcranial direct current stimulation: a role for cortical excitation/inhibition balance? Front Hum Neurosci. 2013;7:602. doi:10.3389/fnhum.2013.00602
   PubMed Web of Science ®Google Scholar
• Ngernyam N, Jensen MP, Auvichayapat N, Punjaruk W, Auvichayapat P. Transcranial direct current stimulation in neuropathic pain. J Pain Relief. 2013;Suppl 3. doi:10.4172/2167-0846.S3-001
   PubMedGoogle Scholar