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Contribution of central neuroplasticity to pathological pain: review of clinical and experimental evidence

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Coderre, Terence J., Katz, Joel, Vaccarino, Anthony L., Melzack, Ronald·1993·Pain

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Abstract

Peripheral tissue damage or nerve injury often leads to pathological pain processes, such as spontaneous pain, hyperalgesia and allodynia, that persist for years or decades after all possible tissue healing has occurred. Although peripheral neural mechanisms, such as nociceptor sensitization and neuroma formation, contribute to these pathological pain processes, recent evidence indicates that changes in central neural function may also play a significant role. In this review, we examine the clinical and experimental evidence which points to a contribution of central neural plasticity to the development of pathological pain. We also assess the physiological, biochemical, cellular and molecular mechanisms that underlie plasticity induced in the central nervous system (CNS) in response to noxious peripheral stimulation. Finally, we examine theories which have been proposed to explain how injury or noxious stimulation lead to alterations in CNS function which influence subsequent pain experience.

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“One component which in ̄uences perceived pain is central sensitization (Woolf 1983; Cook et al., 1987; Coderre et al., 1993).”
Influential
Relief of Glossopharyngeal Neuralgia by Ketamine-induced /V-Methyl-aspartate Receptor Blockade
Eide, P. K., & Stubhaug, A. (1997) · Neurosurgery · doi:10.1097/00006123-199708000-00043 · Cited by 49
Fibromyalgia falls foul of a fallacy
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The Preoperative Administration of Intravenous Dextromethorphan Reduces Postoperative Morphine Consumption
Chia, Y., Liu, K., Chow, L., & Lee, T.-Y. (1999) · Anesthesia & Analgesia · doi:10.1097/00000539-199909000-00041 · Cited by 49
“One strategy for relieving postoperative pain is to prevent or minimize central sensitization ( 1 ,2).”
Background
Fibromyalgia Syndrome
Shim, J. C. (2004) · The Korean journal of pain · doi:10.3344/kjp.2004.17.s.s80 · Cited by 49
Beneficial effects of fibrin glue (Quixil) versus Lichtenstein conventional technique in inguinal hernia repair: a randomized clinical trial
Bracale, U. M., Rovani, M., Picardo, A., Merola, G., Pignata, G., Sodo, M., Salvo, E. D., Ratto, E. L., Noceti, A., Melillo, P., et al. (2012) · Hernia · doi:10.1007/s10029-012-1020-4 · Cited by 48
Amitriptyline induces nuclear transcription factor-κB–dependent glutamate transporter upregulation in chronic morphine-infused rats
Tai, Y.-H., Tsai, R.-Y., Wang, Y.-H., Cherng, C., Tao, P., Liu, T.-M., & Wong, C. ‐. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.02.055 · Cited by 48
Effect of Treatment on Trigger Points
Majlesi, J., & Unalan, H. (2010) · Current pain and headache reports · doi:10.1007/s11916-010-0132-8 · Cited by 56
Intercostal Muscle Flap for Decreasing Pain After Thoracotomy: A Prospective Randomized Trial
Allama, A. M. (2009) · The Annals of Thoracic Surgery · doi:10.1016/j.athoracsur.2009.07.094 · Cited by 48
Analgesic and anti‐hyperalgesic effects of muscle injections with lidocaine or saline in patients with fibromyalgia syndrome
Staud, R. M., Weyl, E. E., Bartley, E. J., Price, D. D., & Robinson, M. E. (2013) · European Journal of Pain · doi:10.1002/j.1532-2149.2013.00422.x · Cited by 48
“This lack of effectiveness of lidocaine on clinical pain ratings is puzzling because hyperalgesia represents an important mechanism for clinical pain (Coderre et al., 1993; Mannion and Woolf, 2000; Staud et al., 2012).”
Background
Muscle Pain Syndromes
Hong, C. (2011) · Elsevier eBooks · doi:10.1016/b978-1-4377-0884-4.10043-6 · Cited by 32
Efficacy and Safety of Dextromethorphan/Quinidine at Two Dosage Levels for Diabetic Neuropathic Pain: A Double-Blind, Placebo-Controlled, Multicenter Study
Shaibani, A. I., Pope, L. E., Thisted, R. A., & Hepner, A. (2012) · Pain Medicine · doi:10.1111/j.1526-4637.2011.01316.x · Cited by 48
Predicting outcome of TENS in chronic pain: A prospective, randomized, placebo controlled trial
Oosterhof, J., Samwel, H. J. A., de Boo, T. M., Wilder‐Smith, O. H. G., Oostendorp, R. A. B., & Crul, B. J. P. (2007) · Pain · doi:10.1016/j.pain.2007.06.009 · Cited by 48
“…remainder of patients was classified as ‘‘Injury of bone and soft tissue and visceral pain disorders’’ (IBST) – assuming self-sustaining central hyperexcitability (Coderre et al., 1993), as there were no signs of inflammation or peripheral nerve lesions, for visceral pain disorders it is…”
BackgroundInfluential
Critical role of the capsaicin-sensitive nerve fibers in the development of the causalgic symptoms produced by transecting some but not all of the nerves innervating the rat tail
Kim, Y. I., Na, H., Han, J., & Sk, H. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-06-04133.1995 · Cited by 48
“…capsaicin of AS-and C-fibers prevented the activities induced in these fibers by the nerve injury from producing " central sensitization, " central changes thought to be required for the emergence of neuropathic pain symptoms following peripheral nerve injury (Roberts, 1986; Coderre et al., 1993).”
Dynamic mechanical allodynia in humans is not mediated by a central presynaptic interaction of A β -mechanoreceptive and nociceptive C-afferents
Wasner, G. L., Baron, R., & Jänig, W. (1999) · Pain · doi:10.1016/s0304-3959(98)00159-6 · Cited by 48
Increased expression of growth-associated protein (GAP-43) in lower urinary tract pathways following cyclophosphamide (CYP)-induced cystitis
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Hyperexcitability in sensory neurons of rats selected for high versus low neuropathic pain phenotype
Liu, C., Raber, P., Ziv-Sefer, S., & Devor, M. G. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00161-0 · Cited by 48
The Dose-Response Relationship of Ketorolac as a Component of Intravenous Regional Anesthesia with Lidocaine
Steinberg, R. B., Reuben, S. S., & Gardner, G. (1998) · Anesthesia & Analgesia · doi:10.1213/00000539-199804000-00021 · Cited by 48
Pain threshold and sleep quality in women with endometriosis
Nunes, F. R., Ferreira, J. M., & Bahamondes, L. (2015) · European Journal of Pain · doi:10.1002/ejp.514 · Cited by 46
“Those findings showed that endometriosis is associated with central sensitization of the neural structures involved in pain perception, which occurs as a consequence of biochemical, cellular and molecular disorders of the pain perception mechanisms (Coderre et al., 1993).”
Background
Activation of spinal phosphatidylinositol 3-kinase/protein kinase B mediates pain behavior induced by plantar incision in mice
Xu, B. Y., Guan, X., Jun-xiong, Y., Lv, J., Zhang, H., Fu, Q., Xiang, H., Bu, H., Shi, D., Shu, B., et al. (2014) · Experimental Neurology · doi:10.1016/j.expneurol.2014.02.019 · Cited by 47
“Therefore mapping Fos expression in these neurons is the best biomarker to indicate the activity of these neurons (Coderre et al., 1993; Coggeshall, 2005; Ghanima et al., 2002; Ma and Woolf, 1996; Ruan et al., 2010).”
Effects of the suppression of acute herpetic pain by gabapentin and amitriptyline on the incidence of delayed postherpetic pain in mice
Kuraishi, Y., Takasaki, I., Nojima, H., Shiraki, K., & Takahata, H. (2004) · Life Sciences · doi:10.1016/j.lfs.2004.01.005 · Cited by 47
Impact of haloperidol and risperidone on gene expression profile in the rat cortex
Fehér, L. Z., Kalman, J. L., Puskás, L. G., Gyülvészi, G., Kitajka, K., Penke, B., Palotás, M., Samarova, E. I., Molnár, J., Zvara, Á., et al. (2005) · Neurochemistry International · doi:10.1016/j.neuint.2005.04.020 · Cited by 47
Influence of formalin concentration on the antinociceptive effects of anti‐inflammatory drugs in the formalin test in rats: Separate mechanisms underlying the nociceptive effects of low‐and high‐concentration formalin
Yashpal, K., & Coderre, T. J. (1998) · European Journal of Pain · doi:10.1016/s1090-3801(98)90047-7 · Cited by 47
“Earlyphase (O-5 min) and late-phase (25-60 min) nociceptive responses to formalin were assessed using the weighted-scores method of behavioural rating (Coderre et al., 1993~).”
BackgroundMethodSelf-citation
Early Nociceptive Events Influence the Temporal Profile, but not the Magnitude, of the Tonic Response to Subcutaneous Formalin: Effects with Remifentanil
Taylor, B. K., Peterson, M. A., & Basbaum, A. I. (1997) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(24)36429-8 · Cited by 47
A study to evaluate buprenorphine at 40 μg kg−1 compared to 20 μg kg−1 as a post-operative analgesic in the dog
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Prospects for Metabotropic Glutamate 1 Receptor Antagonists in the Treatment of Neuropathic Pain
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Evaluation of lidocaine treatment on frequency of cardiac arrhythmias, acute kidney injury, and hospitalization time in dogs with gastric dilatation volvulus
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Trigeminal neuroplasticity underlies allodynia in a preclinical model of mild closed head traumatic brain injury (cTBI)
Mustafa, G., Hou, J., Tsuda, S., Nelson, R., Sinharoy, A., Wilkie, Z., Pandey, R., Caudle, R. M., Neubert, J. K., Thompson, F. J., et al. (2016) · Neuropharmacology · doi:10.1016/j.neuropharm.2016.03.016 · Cited by 46
“It is a hypothesis that such changes could underlie the observed alterations in thermosensitivity [22; 63].”
Lack of efficacy of riluzole in the treatment of peripheral neuropathic pain conditions
Galer, B. S., Twilling, L., Harle, J., Cluff, R. S., Friedman, E., & Rowbotham, M. C. (2000) · Neurology · doi:10.1212/wnl.55.7.971 · Cited by 46
Mechanisms of Pavlovian conditioning: Role of protection from habituation in spinal conditioning.
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Methadone for Phantom Limb Pain
Bergmans, L., Snijdelaar, D. G., Katz, J. D., & Crul, B. J. P. (2002) · Clinical Journal of Pain · doi:10.1097/00002508-200205000-00012 · Cited by 46
Self-citation
Pain During Injection of Propofol: The Effect of Prior Administration of Butorphanol
Agarwal, A., Raza, M., Dhiraaj, S., Pandey, R. K., Gupta, D. K., Pandey, C. K., Singh, P. K., & Singh, U. (2004) · Anesthesia & Analgesia · doi:10.1213/01.ane.0000117002.03919.49 · Cited by 46
The preoperative administration of ketoprofen improves analgesia after laparoscopic cholecystectomy in comparison with propacetamol or postoperative ketoprofen
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Nimesulide — Actions and Uses
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Authors: Coderre, T. J., Katz, J., Vaccarino, A. L., & Melzack, R.
Affiliations: University of Toronto (CA)
LSU New Orleans (US)
McGill University (CA)
Corresponding author: Vaccarino, Anthony L.
ORCID: Coderre, Terence J.
Katz, Joel
Vaccarino, Anthony L.
Venue: Pain
Publisher: Ovid Technologies (Wolters Kluwer Health)
Published: 1993-03
Volume: 52
Issue: 3
Pages: 259-285
ISSN: 0304-3959 (ISSN-L)
DOI: 10.1016/0304-3959(93)90161-h
OpenAlex: W2062625412
Cited by: 1,966
References: 304
Citations by year: 2026: 2 · 2025: 11 · 2024: 8 · 2023: 16 · 2022: 16 · 2021: 28 · 2020: 24 · 2019: 36 · 2018: 25 · 2017: 25 · 2016: 30 · 2015: 30 · 2014: 37 · 2013: 42 · 2012: 53
FWCI: 12.25
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Pain (publishedVersion)
PubMed (publishedVersion)
YorkSpace (York University) (submittedVersion)
Funders: Medical Research Council Canada
Natural Sciences and Engineering Research Council of Canada (A7891)
Fonds de Recherche du Québec - Santé
Medical Research Council
Topics: Health Sciences › Medicine › Physiology (medical) › Pain Mechanisms and Treatments
Health Sciences › Medicine › Anesthesiology and Pain Medicine › Pain Management and Treatment
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords: pathological pain, hyperalgesia, allodynia, spontaneous pain, central sensitization, nerve injury, nociceptor sensitization, neuroma formation, central nervous system plasticity, noxious stimulation, pain mechanisms
MeSH terms: Acute Disease, Animals, Central Nervous System, Chronic Disease, Humans, Models, Neurological, Neuronal Plasticity, Pain, Palliative Care, Pain Management

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Contribution of central neuroplasticity to pathological pain: review of clinical and experimental evidence

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