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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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“Unrelieved pain can have profound deleterious effects on the cardiovascular, pulmonary, immunological, and nervous systems, and can alter children’s responses to pain later in life.(6,28,34,35) The American Academy of Pediatrics (AAP) and American Pain Society (APS)(1) attribute the lack of effective pain management t…”
Background
Cetamina e analgesia preemptiva
de Oliveira, C. M. B., Sakata, R. K., Issy, A. M., & Garcia, J. B. S. (2004) · Brazilian Journal of Anesthesiology · doi:10.1590/s0034-70942004000500016 · Cited by 33
Peripheral and central nervous changes in patients with rheumatoid arthritis in response to repetitive painful stimulation
Hummel, T. R., Schießl, C., Wendler, J., & Kobal, G. (2000) · International Journal of Psychophysiology · doi:10.1016/s0167-8760(00)00087-8 · Cited by 33
Dextromethorphan and quinidine in adult patients with uncontrolled painful diabetic peripheral neuropathy: A 29-day, multicenter, open-Label, dose-escalation study
Thisted, R. A., Klaff, L. J., Schwartz, S. L., Wymer, J. P., Culligan, N. W., Gérard, G., Pope, L. E., & Berg, J. E. (2006) · Clinical Therapeutics · doi:10.1016/j.clinthera.2006.10.005 · Cited by 31
Pain on injection of propofol: a comparison of methylene blue and lidocaine
Salman, A. E., Salman, M. A., Sarıcaoğlu, F., Akıncı, S. B., & Aypar, Ü. (2011) · Journal of Clinical Anesthesia · doi:10.1016/j.jclinane.2010.09.008 · Cited by 33
“Such action produces venous dilatation and hyperpermeability, which increases contact between the aqueous phase of propofol and free nerve endings, resulting in pain on injection [4,16,17].”
Background
Chronic sleep restriction increases pain sensitivity over time in a periaqueductal gray and nucleus accumbens dependent manner
Sardi, N. F., Lazzarim, M. K., Guilhen, V. A., Marcílio, R. S., Natume, P., Watanabe, T., Lima, M. M. S., Tobaldini, G., & Fischer, L. (2018) · Neuropharmacology · doi:10.1016/j.neuropharm.2018.06.022 · Cited by 35
“c-Fos protein is rapidly and transiently expressed in stimulated neurons in response to elevation of intracellular calcium (Coderre et al., 1993; Lerea et al., 1992).”
Change in excitability and phenotype of substance P and its receptor in cat Aβ sensory neurons following peripheral inflammation
Xu, G., & Zhao, Z. (2001) · Brain Research · doi:10.1016/s0006-8993(01)03203-6 · Cited by 33
The Effect of Preemptive Pudendal Nerve Blockade on Pain After Transvaginal Pelvic Reconstructive Surgery
Abramov, Y., Sand, P. K., Gandhi, S., Botros, S. M., Miller, J. R., Koh, E.-K., & Goldberg, R. P. (2005) · Obstetrics and Gynecology · doi:10.1097/01.aog.0000165275.39905.0d · Cited by 33
“20 Previous prolapse surgery 6 (12) 8 (16) .”
Spinal pathways involved in supraspinal modulation of neuropathic manifestations in rats
Saadé, N. E., Al-Amin, H. A., Chalouhi, S. E., Baki, S. A., Jabbur, S. J., & Atweh, S. (2006) · Pain · doi:10.1016/j.pain.2006.07.010 · Cited by 33
“…2003; Ringkamp and Meyer, 2005); (2) functional and structural changes in the dorsal horn neurons (McMahon and Wall, 1984; Gracely et al., 1992; Coderre et al., 1993; Goff et al., 1998; Shimoyama et al., 2005) and primary afferents (McMahon and Kett-White, 1991; Woolf et al., 1995; Goff et…”
Background
Effects of NMDA receptor antagonists on opioid-induced respiratory depression and acute antinociception in rats
Hoffmann, V. L. H., Vermeyen, K. M., Adriaensen, H. F., & Meert, T. F. (2003) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(03)00020-0 · Cited by 33
Preemptive Use of Ketamine on Post Operative Pain of Appendectomy
Behdad, A., Hosseinpour, M., & Khorasani, P. (2011) · The Korean journal of pain · doi:10.3344/kjp.2011.24.3.137 · Cited by 33
Shock-induced hyperalgesia: IV. Generality.
Meagher, M. W., Ferguson, A. R., Crown, E. D., McLemore, S., King, T. E., Sieve, A. N., & Grau, J. W. (2001) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/0097-7403.27.3.219 · Cited by 33
Pre-emptive Analgesia with Epidural Morphine or Morphine and Bupivacaine
Subramaniam, B., Pawar, D. K., & Kashyap, L. (2000) · Anaesthesia and Intensive Care · doi:10.1177/0310057x0002800406 · Cited by 33
Chapter 15 Involvement of glutamatergic neurotransmission and protein kinase C in spinal plasticity and the development of chronic pain
Tölle, T. R., Berthele, A., Schadrack, J., & Zieglgänsberger, W. (1996) · Progress in brain research · doi:10.1016/s0079-6123(08)62575-3 · Cited by 33
A new model of experimental parotitis in rats and its implication for trigeminal nociception
Ogawa, A., Ren, K., Tsuboi, Y., Morimoto, T., Sato, T., & Iwata, K. (2003) · Experimental Brain Research · doi:10.1007/s00221-003-1538-x · Cited by 33
“…inflammation, which produces a wide variety of changes in the peripheral and central nervous systems, resulting in peripheral and central sensitization (Abbadie and Besson 1992; Abbadie et al. 1992; Coderre et al. 1993; Imbe et al. 1999; Iwata et al. 1998; Ren and Dubner 1999; Zhou et al. 1999).”
BackgroundInfluential
The effects of intrathecal morphine and clonidine on the prevention and reversal of spinal cord hyperexcitability following sciatic nerve section in the rat
Luo, L., Puke, C. M. J., & Wiesenfeld‐Hallin, Z. (1994) · Pain · doi:10.1016/0304-3959(94)90205-4 · Cited by 33
“There is considerable evidence that peripheral nerve injury is associated with the development of spinal hyperexcitability, which may lead to central neuroplasticity contributing to neuropathic pain (see Coderre et al. 1993 for review).”
Background
Epidural Verapamil Reduces Analgesic Consumption After Lower Abdominal Surgery
Choe, H., Kim, J.-S., Ko, S., Kim, D.-C., Han, Y., & Song, H. S. (1998) · Anesthesia & Analgesia · doi:10.1213/00000539-199804000-00020 · Cited by 33
GABAA α5 subunit-containing receptors do not contribute to reversal of inflammatory-induced spinal sensitization as indicated by the unique selectivity profile of the GABAA receptor allosteric modulator NS16085
de Lucas, A. G., Ahring, P. K., Larsen, J. S., Rivera-Arconada, I., Lopez-Garcia, J. A., Mirza, N. R., & Munro, G. (2015) · Biochemical Pharmacology · doi:10.1016/j.bcp.2014.12.010 · Cited by 32
Pituitary-Adrenocortical Responses to Persistent Noxious Stimuli in the Awake Rat: Endogenous Corticosterone Does Not Reduce Nociception in the Formalin Test
Taylor, B. K. (1998) · Endocrinology · doi:10.1210/en.139.5.2407 · Cited by 89
Oral pregabalin reverses cold allodynia in two distinct models of peripheral neuropathic pain
Gustafsson, H., & Sandin, J. (2009) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2009.01.014 · Cited by 32
Evaluation of analgesia provided by the administration of epidural ketamine in dogs with a chemically induced synovitis
Hamilton, S. M., Johnston, S. A., & Broadstone, R. V. (2005) · Veterinary Anaesthesia and Analgesia · doi:10.1111/j.1467-2995.2004.00171.x · Cited by 32
Management of vulvar pain
Fischer, G. O. (2004) · Dermatologic Therapy · doi:10.1111/j.1396-0296.2004.04014.x · Cited by 32
Anatomy and physiology of chronic pain
Rosenow, J. M., & Henderson, J. M. (2003) · Neurosurgery Clinics of North America · doi:10.1016/s1042-3680(03)00009-3 · Cited by 32
α5GABAAReceptors Mediate Tonic Inhibition in the Spinal Cord Dorsal Horn and Contribute to the Resolution Of Hyperalgesia
Pérez-Sánchez, J., Lorenzo, L.-É., Lecker, I., Zurek, A. A., Labrakakis, C., Bridgwater, E. M., Orser, B. A., Koninck, Y. D., & Bonin, R. P. (2016) · Journal of Neuroscience Research · doi:10.1002/jnr.23981 · Cited by 32
“Here we show that the activity of a5GABAARs in the spinal cord regulates the late phase of the formalin test, which is associated with central sensitization (Coderre et al., 1993).”
BackgroundInfluential
The emergence of animal models of chronic pain and logistical and methodological issues concerning their use
Coderre, T. J., & Laferrière, A. (2019) · Journal of Neural Transmission · doi:10.1007/s00702-019-02103-y · Cited by 32
Self-citation
The effect of spinal manipulation on brain neurometabolites in chronic nonspecific low back pain patients: a randomized clinical trial
Didehdar, D., Kamali, F., Yoosefinejad, A. K., & Lotfi, M. (2019) · Irish Journal of Medical Science (1971 -) · doi:10.1007/s11845-019-02140-2 · Cited by 33
Chapter 24 Referred pain from internal organs
Giamberardino, M. A., Affaitati, G., & Costantini, R. (2006) · Handbook of clinical neurology · doi:10.1016/s0072-9752(06)80028-x · Cited by 32
“Some authors claim that this phenomenon is an indicator that central plastic changes, once established, may persist, becoming relatively independent of the primary triggering event (Coderre et al., 1992).”
Background
Le dysfonctionnement du « brain-gut »
Bonaz, B. L., & Sabaté, J. (2009) · Gastroentérologie Clinique et Biologique · doi:10.1016/s0399-8320(09)71525-8 · Cited by 33
The transcription factor ΔFosB is recruited by inflammatory pain
Luis‐Delgado, O. E., Barrot, M., Rodeau, J., Ulery, P. G., Freund‐Mercier, M. J., & Lasbennes, F. (2006) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2006.03970.x · Cited by 34
An evaluation of the anti-inflammatory, antipyretic and analgesic effects of hydroethanol leaf extract ofAlbizia zygiain animal models
Abotsi, W. K. M., Lamptey, S. B., Afrane, S., Boakye‐Gyasi, E., Umoh, R. U., & Woode, E. (2016) · Pharmaceutical Biology · doi:10.1080/13880209.2016.1262434 · Cited by 32
“…phase (inflammatory pain), reflecting ongoing activity in primary afferents and central sensitization of spinal cord circuits secondary to the barrage of input that occurs during the first phase (Dubuisson & Dennis 1977; Tjolsen et al. 1992; Coderre et al. 1993; McNamara et al. 2007; Figure 5.”
Background
Neuromodulation with electromagnetic stimulation for seizure suppression: From electrode to magnetic coil
Ye, H., & Kaszuba, S. V. (2019) · IBRO Reports · doi:10.1016/j.ibror.2019.06.001 · Cited by 32
Ziconotide: A new pharmacological class of drug for the management of pain
Mathur, V. S. (2000) · Seminars in Anesthesia Perioperative Medicine and Pain · doi:10.1053/sa.2000.6787 · Cited by 32
When There Is No Benchmark
Donovan, M. I., Evers, K., Jacobs, P., & Mandleblatt, S. (1999) · Journal of Pain and Symptom Management · doi:10.1016/s0885-3924(99)00021-4 · Cited by 32
Risk and Prognostic Factors of Postherpetic Neuralgia and Focal Sensory Denervation: A Prospective Evaluation in Acute Herpes Zoster Ophthalmicus
Zaal, M. J. W., Völker-Dieben, H. J. M., & D'Amaro, J. (2000) · Clinical Journal of Pain · doi:10.1097/00002508-200012000-00012 · Cited by 32
Effect of ketamine on spinal cord nociceptive transmission in normal and monoarthritic rats
Laurido, C., Pélissier, T., Pérez, H., Flores, F. J., & Hernández, A. (2001) · Neuroreport · doi:10.1097/00001756-200106130-00008 · Cited by 32
Pain in the 21st Century: The Neuromatrix and Beyond
Melzack, R., & Katz, J. D. (2006) · Kluwer Academic Publishers eBooks · doi:10.1007/0-387-25610-5_7 · Cited by 33
“Nerve injury can also lead to the development of increased neuronal activity at various levels of the somatosensory system (see review by Coderre et al., 1993 ).”
BackgroundSelf-citation

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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