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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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“Hyperexcitability of the nociceptive processing regions of the central nervous system (CNS) has been implicated as a putative pathophysiological mechanism underlying different types of chronic pain (Dubner, 1991; Coderre et al., 1993).”
Evidence for Shared Pain Mechanisms in Osteoarthritis, Low Back Pain, and Fibromyalgia
Staud, R. M. (2011) · Current Rheumatology Reports · doi:10.1007/s11926-011-0206-6 · Cited by 174
“Prolonged activation of polymodal nociceptors can result in central hyperexcitability of dorsal horn neurons manifested by lowered pain thresholds, responding to non-noxious stimuli, prolonged after-sensations, and expansion of receptive fields [ 3 ].”
Background
The mediation of disability by self efficacy in different samples of chronic pain patients
Arnstein, P. (2000) · Disability and Rehabilitation · doi:10.1080/09638280050200296 · Cited by 191
Progressive tactile hypersensitivity: an inflammation-induced incremental increase in the excitability of the spinal cord
Ma, Q., & Woolf, C. J. (1996) · Pain · doi:10.1016/0304-3959(96)03105-3 · Cited by 174
Effect of inhibition of nitric oxide synthase on chronic tension-type headache: a randomised crossover trial
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Duration of leg pain as a predictor of outcome after surgery for lumbar disc herniation: a prospective cohort study with 1-year follow up
Nygaard, O. P., Kloster, R., & Solberg, T. K. (2000) · Journal of Neurosurgery Spine · doi:10.3171/spi.2000.92.2.0131 · Cited by 174
Peripheral and central sensitization in fibromyalgia: Pathogenetic role
Staud, R. M., & Smitherman, M. L. (2002) · Current Pain and Headache Reports · doi:10.1007/s11916-002-0046-1 · Cited by 173
“One study showed that activation of NMDA receptors in the spinal cord causes the release of SP and dramatic structural changes in the dendrites of neurons that display SP receptors [ 67 ].”
Background
Central Hypersensitivity in Chronic Pain: Mechanisms and Clinical Implications
Curatolo, M., Arendt‐Nielsen, L., & Petersen‐Felix, S. (2006) · Physical Medicine and Rehabilitation Clinics of North America · doi:10.1016/j.pmr.2005.12.010 · Cited by 173
Similarities between severe tinnitus and chronic pain
Moller, A. R. (2000) · Journal of the American Academy of Audiology · doi:10.1055/s-0042-1748038 · Cited by 240
“The neural mechanisms of chronic pain are different from that of acute pain (Price et al, 1992 ; Coderre et al, 1993), and the neural abnormality that causes severe tinnitus may be different from that causing mild to moderate tinnitus .”
BackgroundInfluential
Genetic impairment of interleukin-1 signaling attenuates neuropathic pain, autotomy, and spontaneous ectopic neuronal activity, following nerve injury in mice
Wolf, G., Gabay, E., Tal, M., Yirmiya, R., & Shavit, Y. (2006) · Pain · doi:10.1016/j.pain.2005.11.011 · Cited by 171
“…and in the dorsal root ganglion (DRG) (Kajander et al., 1992; Liu et al., 2000a) not only parallels the development of neuropathic pain (Draganic et al., 2001; Liu et al., 2000a), but also appears to trigger and maintain spinal central sensitization (Coderre et al., 1993; Woolf et al., 1992).”
Background
Changes in the concentrations of amino acids in the cerebrospinal fluid that correlate with pain in patients with fibromyalgia: implications for nitric oxide pathways
Larson, A. A., Giovengo, S. L., Russell, J. I., & Michalek, J. E. (2000) · Pain · doi:10.1016/s0304-3959(00)00284-0 · Cited by 171
“Pathological pain of this type has been postulated to result from peripheral sensitization of primary afferent nociceptors (Campbell and Meyer, 1983; Raja et al., 1984) and/or central sensitization involving increased excitability of neurons in the spinal cord (Woolf, 1983; Coderre et al., 1993).”
Background
Continued disability and pain after lumbar disc surgery: The role of cognitive-behavioral factors
den Boer, J. J., Oostendorp, R. A. B., Beems, T., Munneke, M., & Evers, A. W. M. (2006) · Pain · doi:10.1016/j.pain.2006.02.008 · Cited by 178
“There is preliminary evidence that continuing nociception is associated with alterations in the peripheral and central processing of pain (Coderre et al., 1993; Woolf and Chong, 1993; Wilder-Smith et al., 2002).”
Background
Initiating Mechanisms of Experimentally Induced Tension-Type Headache
Jensen, R., & Olesen, J. (1996) · Cephalalgia · doi:10.1046/j.1468-2982.1996.1603175.x · Cited by 169
Pharmacological classification of central post-stroke pain: comparison with the results of chronic motor cortex stimulation therapy
Yamamoto, T., Katayama, Y., Hirayama, T., & Tsubokawa, T. (1997) · Pain · doi:10.1016/s0304-3959(97)00028-6 · Cited by 168
“Recent evidence has suggested that EAAs play an important role in such hyperactivities, especially after sensory deafferentation (Nestler and Greengard, 1983; Schaible et al., 1991; Coderre and Melzack, 1991; Coderre et al., 1993; Marszalec and Narahashi, 1993).”
Background
Spinal brain-derived neurotrophic factor (BDNF) produces hyperalgesia in normal mice while antisense directed against either BDNF or trkB, prevent inflammation-induced hyperalgesia
Groth, R. D., & Aanonsen, L. (2002) · Pain · doi:10.1016/s0304-3959(02)00264-6 · Cited by 168
“Though most often thought of as a mechanism for memory formation, LTP mimics many characteristics associated with chronic pain, and thus may serve as a common paradigm for the cellular and molecular changes underlying central sensitization (Coderre et al., 1993).”
Kainate GluR5 receptor subtype mediates the nociceptive response to formalin in the rat
Simmons, R. M. A., Li, D. L., Hoo, K. H., Deverill, M., Ornstein, P. L., & Iyengar, S. (1998) · Neuropharmacology · doi:10.1016/s0028-3908(97)00188-3 · Cited by 168
Central Sensitivity Syndromes: Mounting Pathophysiologic Evidence to Link Fibromyalgia with Other Common Chronic Pain Disorders
Kindler, L. L., Bennett, R. M., & Jones, K. D. (2009) · Pain Management Nursing · doi:10.1016/j.pmn.2009.10.003 · Cited by 167
Phantom Limb Pain
Hill, A. (1999) · Journal of Pain and Symptom Management · doi:10.1016/s0885-3924(98)00136-5 · Cited by 166
Opioid analgesics as noncompetitive N-methyl-d-aspartate (NMDA) antagonists
Ebert, B., Thorkildsen, C., Andersen, S., Christrup, L. L., & Hjeds, H. (1998) · Biochemical Pharmacology · doi:10.1016/s0006-2952(98)00088-4 · Cited by 164
“Based on this hypothesis, several potent and selective noncompetitive NMDA antagonists have been investigated in animal models of neuropathic pain [5, 14–16].”
Background
T‐type voltage‐gated calcium channels as targets for the development of novel pain therapies
Todorovic, S. M., & Jevtović‐Todorović, V. (2011) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2011.01256.x · Cited by 163
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Background
Recent and forgotten aspects of visceral pain
Giamberardino, M. A. (1999) · European Journal of Pain · doi:10.1053/eujp.1999.0117 · Cited by 163
Expanding the biological basis of tinnitus: crossmodal origins and the role of neuroplasticity
Cacace, A. T. (2003) · Hearing Research · doi:10.1016/s0378-5955(02)00717-7 · Cited by 161
Prevalence of cervical spinal pain in craniomandibular pain patients
Visscher, C. M., Lobbezoo, F., Boer, W. D., van der Zaag, J., & Naeije, M. (2001) · European Journal Of Oral Sciences · doi:10.1034/j.1600-0722.2001.00996.x · Cited by 162
The role of excitatory amino acid receptors and intracellular messengers in persistent nociception after tissue injury in rats
Coderre, T. J. (1993) · Molecular Neurobiology · doi:10.1007/bf02769177 · Cited by 161
“Recent evidence suggests that following tissue injury there are specific changes in central neuron function that contribute to persistent pain or nociception (see Woolf, 1991; Dubner and Ruda, 1992; Coderre et al., 1993 for reviews).”
Self-citation
The Effects of Ketamine on the Temporal Summation (Wind-Up) of the RIII Nociceptive Flexion Reflex and Pain in Humans
Guirimand, F., Dupont, X., Brasseur, L., CHAUVIN, M., & Bouhassira, D. (2000) · Anesthesia & Analgesia · doi:10.1097/00000539-200002000-00031 · Cited by 160
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The Endogenous Redox Agent L-Cysteine Induces T-Type Ca2+ Channel-Dependent Sensitization of a Novel Subpopulation of Rat Peripheral Nociceptors
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“…described in A–G. Firing was triggered by a 2 ms, 1.7 nA stimulus from a membrane potential of 65 mV. the spinal cord, which is a suggested physiological correlate for neuropathic pain (for review, see Levine et al., 1993) (Coderre et al., 1993; Caterina and Julius, 2001; Bhave and Gereau, 2004).”
BackgroundInfluential
Limbically Augmented Pain Syndrome (LAPS): Kindling, Corticolimbic Sensitization, and the Convergence of Affective and Sensory Symptoms in Chronic Pain Disorders
Rome, H. P., & Rome, J. D. (2000) · Pain Medicine · doi:10.1046/j.1526-4637.2000.99105.x · Cited by 158
Transcutaneous electrical nerve stimulation (TENS) for chronic low-back pain
Milne, S., Welch, V. A., Brosseau, L., Saginur, M., Shea, B., Tugwell, P., & Wells, G. (2000) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd003008 · Cited by 158
Peripheral nerve exposure to HIV viral envelope protein gp120 induces neuropathic pain and spinal gliosis
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Mislocalization of tactile stimulation in patients with complex regional pain syndrome
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“Nociceptive input might induce such cortical changes [3, 8, 9, 28].”
Background
Blockade of spinal N- and P-type, but not L-type, calcium channels inhibits the excitability of rat dorsal horn neurones produced by subcutaneous formalin inflammation
Díaz, Á., & Dickenson, A. H. (1997) · Pain · doi:10.1016/s0304-3959(96)03271-x · Cited by 154
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Background
Randomized Prospective Study Comparing Preoperative Epidural and Intraoperative Perineural Analgesia for the Prevention of Postoperative Stump and Phantom Limb Pain Following Major Amputation
Lambert, A. W., Dashfield, A. K., Cosgrove, C., Wilkins, D. C., Walker, A. J., & Ashley, S. (2001) · Regional Anesthesia & Pain Medicine · doi:10.1053/rapm.2001.23934 · Cited by 154
“Postamputation pain was classified as previously described: stump pain referred to the stump and phantom pain to any painful sensation associated with the missing limb.16 VAS scores were averaged at 6-hour intervals.”
BackgroundInfluential
Amitriptyline suppresses neuroinflammation and up-regulates glutamate transporters in morphine-tolerant rats
Tai, Y.-H., Wang, Y.-H., Wang, J., Tao, P., Tung, C., & Wong, C. (2006) · Pain · doi:10.1016/j.pain.2006.03.018 · Cited by 150
“, 1996), and chronic pain-associated hyperalgesia (Coderre et al., 1993; Urban and Gebhart, 1998; Porreca et al., 2002).”
Background
Grading of monosodium iodoacetate-induced osteoarthritis reveals a concentration-dependent sensitization of nociceptors in the knee joint of the rat
Schuelert, N., & McDougall, J. J. (2009) · Neuroscience Letters · doi:10.1016/j.neulet.2009.08.063 · Cited by 150
“[4] T.”
Background
Painful and Nonpainful Phantom and Stump Sensations in Acute Traumatic Amputees
Schley, M. T., Wilms, P., Töpfner, S., Schaller, H.-P., Schmelz, M., Konrad, C. J., & Birbaumer, N. (2008) · The Journal of Trauma: Injury, Infection, and Critical Care · doi:10.1097/ta.0b013e31812eed9e · Cited by 149
“Always 2 (7) 5 (14) 5 (13) 14 (28) A few times per day 4 (14) 7 (20) 8 (20) 7 (14) A few times per week 6 (21) 5 (14) 7 (18) 5 (10) A few times per month 6 (21) 8 (23) 6 (15) 12 (24) Less than 1 time per month 9 (31) 6 (17) 12 (30) 8 (16) Unknown 2 (7) 4 (11) 2 (5) 5 (10) Dynamics of pain or sensation (after first occ…”

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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