Chronic pain after clip-compression injury of the rat spinal cord
Abstract
Chronic tactile allodynia and hyperalgesia are frequent complications of spinal cord injury (SCI) with poorly understood mechanisms. Possible causes are plastic changes in the central arbors of nociceptive and nonnociceptive primary sensory neurons and changes in descending modulatory serotonergic pathways. A clinically relevant clip-compression model of SCI in the rat was used to investigate putative mechanisms of chronic pain. Behavioral testing (n = 18 rats) demonstrated that moderate (35 g) or severe (50 g) SCI at the 12th thoracic spinal segment (T-12) reliably produces chronic tactile allodynia and hyperalgesia that can be evoked from the hindpaws and back. Quantitative morphometry (n = 37) revealed no changes after SCI in the density or distribution of Abeta-, Adelta-, and C-fiber central arbors of primary sensory neurons within the thoracolumbar segments T-6 to L-4. This observation rules out a mandatory relationship between pain-related behaviors and changes in the distribution or density of central afferent arbors. The area of serotonin immunoreactivity in the dorsal horn (n = 12) decreased caudal to the injury site (L1-4) and increased threefold rostral to it (T9-11). The decreased serotonin and presence of tactile allodynia and hyperalgesia caudal to the injury are consistent with disruption of descending antinociceptive serotonergic tracts that modulate pain transmission. The functional significance of the increased serotonin in rostral segments may relate to the development of tactile allodynia as serotonin also has known pronociceptive actions. Changes in the descending serotonergic pathway require further investigation, as a disruption of the balance of serotonergic input rostral and caudal to the injury site may contribute to the etiology of chronic pain after SCI.
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Spinal cord injury produces mechanical hyperalgesia and allodynia.
“Spinal cord injury (SCI)102 produces mechanical hyperalgesia and allodynia.”
From Cannabinoids as Pharmacotherapies for Neuropathic Pain: From the Bench to the Bedside (2009) · cites this paper as [102]
Cites
Pain mechanisms: a new theory.
Melzack, R., & Wall, P. D. (1965) · Science · doi:10.1126/science.150.3699.971 · Cited by 11,108 · see citing works
A Sensitive and Reliable Locomotor Rating Scale for Open Field Testing in Rats
Basso, D. M., Beattie, M. S., & Bresnahan, J. C. (1995) · Journal of Neurotrauma · doi:10.1089/neu.1995.12.1 · Cited by 4,481 · see citing works
Neurotransmitters in Nociceptive Modulatory Circuits
Fields, H. L., Heinricher, M. M., & Mason, P. (1991) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.14.030191.001251 · Cited by 992 · see citing works
Primary Structure And Functional Expression of the 5HT 3 Receptor, A Serotonin-gated Ion Channel
Maricq, A. V., Peterson, A. S., Brake, A. J., Myers, R., & Julius, D. J. (1991) · Science · doi:10.1126/science.1718042 · Cited by 978 · see citing works
Tackling Pain at the Source: New Ideas about Nociceptors
Snider, W. D., & McMahon, S. B. (1998) · Neuron · doi:10.1016/s0896-6273(00)81003-x · Cited by 853 · see citing works
Fehlings, M. G., & Tator, C. H. (1995) · Experimental Neurology · doi:10.1016/0014-4886(95)90027-6 · Cited by 405 · see citing works
Murray, M., & Goldberger, M. E. (1974) · The Journal of Comparative Neurology · doi:10.1002/cne.901580103 · Cited by 378 · see citing works
Bregman, B. S., McAtee, M., Dai, H., & Kuhn, P. L. (1997) · Experimental Neurology · doi:10.1006/exnr.1997.6705 · Cited by 377 · see citing works
Zeitz, K. P., Guy, N., Malmberg, A. B., Dirajlal, S., Martin, W. J., Sun, L. M., Bonhaus, D. W., Stucky, C. L., Julius, D. J., & Basbaum, A. I. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-03-01010.2002 · Cited by 376 · see citing works
Dougherty, K. D., Dreyfus, C., & Black, I. (2000) · Neurobiology of Disease · doi:10.1006/nbdi.2000.0318 · Cited by 373 · see citing works
Widenfalk, J., Lundströmer, K., Jubran, M., Brené, S., & Olson, L. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-10-03457.2001 · Cited by 286 · see citing works
Mechanical and thermal allodynia in chronic central pain following spinal cord injury
Christensen, M. D., Everhart, A. W., Pickelman, J. T., & Hulsebosch, C. E. (1996) · Pain · doi:10.1016/s0304-3959(96)03224-1 · Cited by 286 · see citing works
Agrawal, S., & Fehlings, M. G. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-02-00545.1996 · Cited by 284 · see citing works
Rintala, D. H., Loubser, P. G., Castro, J., Hart, K. A., & Führer, M. J. (1998) · Archives of Physical Medicine and Rehabilitation · doi:10.1016/s0003-9993(98)90032-6 · Cited by 275 · see citing works
Sprouting of primary afferent fibers after spinal cord transection in the rat
Krenz, N. R., & Weaver, L. C. (1998) · Neuroscience · doi:10.1016/s0306-4522(97)00622-2 · Cited by 268 · see citing works
Self-citationBradbury, E. J., Khemani, S., Von, R., King, Priestley, J. V., & McMahon, S. B. (1999) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1999.00809.x · Cited by 243 · see citing works
Chronic pain/dysaesthesiae in spinal cord injury patients: results of a multicentre study
Störmer, S., Gerner, H. J., Grüninger, W., Metzmacher, K., Föllinger, S., Wienke, C., Aldinger, W., Walker, N., Zimmermann, M., & Paeslack, V. (1997) · Spinal Cord · doi:10.1038/sj.sc.3100411 · Cited by 231 · see citing works
Krenz, N. R., Meakin, S. O., Krassioukov, A. V., & Weaver, L. C. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-17-07405.1999 · Cited by 216 · see citing works
Self-citationChristensen, M. D., & Hulsebosch, C. E. (1997) · Experimental Neurology · doi:10.1006/exnr.1997.6608 · Cited by 191 · see citing works
Nashmi, R., & Fehlings, M. G. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00009-4 · Cited by 186 · see citing works
Characterization of chronic pain and somatosensory function in spinal cord injury subjects
Defrin, R., Ohry, A., Blumen, N., & Urca, G. (2001) · Pain · doi:10.1016/s0304-3959(00)00369-9 · Cited by 184 · see citing works
Bregman, B. S. (1987) · Developmental Brain Research · doi:10.1016/0165-3806(87)90213-6 · Cited by 176 · see citing works
Weaver, L. C., Verghese, P. P., Bruce, J. C., Fehlings, M. G., Krenz, N. R., & Marsh, D. R. (2001) · Journal of Neurotrauma · doi:10.1089/08977150152693782 · Cited by 171 · see citing works
Self-citationFehlings, M. G., Tator, C. H., & Linden, R. D. (1989) · Journal of neurosurgery · doi:10.3171/jns.1989.71.3.0403 · Cited by 164 · see citing works
Gould, H. J., Gould, T. N., England, J. D., Paúl, D., Liu, Z. P., & Levinson, S. R. (2000) · Brain Research · doi:10.1016/s0006-8993(99)02216-7 · Cited by 162 · see citing works
Cui, M., Feng, Y., McAdoo, D. J., & Willis, W. D. (1999) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(24)38213-8 · Cited by 151 · see citing works
Hains, B. C., Everhart, A. W., Fullwood, S. D., & Hulsebosch, C. E. (2002) · Experimental Neurology · doi:10.1006/exnr.2002.7892 · Cited by 151 · see citing works
Dual effect of serotonin on formalin-induced nociception in the rat spinal cord
Oyama, T., Ueda, M., Kuraishi, Y., Akaike, A., & Satoh, M. (1996) · Neuroscience Research · doi:10.1016/0168-0102(96)01034-6 · Cited by 135 · see citing works
Eide, P. K., & Hole, K. (1993) · Cephalalgia · doi:10.1046/j.1468-2982.1993.1302075.x · Cited by 117 · see citing works
Kohama, I., Ishikawa, K., & Kocsis, J. D. (2000) · PubMed · Cited by 114 · see citing works
Alterations in AMPA Receptor Subunit Expression after Experimental Spinal Cord Contusion Injury
Grossman, S. D., Wolfe, B., Yasuda, R., & Wrathall, J. R. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-14-05711.1999 · Cited by 108 · see citing works
Ali, Z., Wu, G., Kozlov, A., & Barasi, S. (1996) · Neuroscience Letters · doi:10.1016/0304-3940(95)12600-7 · Cited by 107 · see citing works
Changes in NMDA Receptor Subunit Expression in Response to Contusive Spinal Cord Injury
Bloom, S., Wolfe, B. B., Yasuda, R. P., & Wrathall, J. R. (2000) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2000.0750174.x · Cited by 104 · see citing works
Kohama, I., Ishikawa, K., & Kocsis, J. D. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-04-01538.2000 · Cited by 100 · see citing works
Two-Tiered Inhibition of Axon Regeneration at the Dorsal Root Entry Zone
Ramer, M. S., Duraisingam, I., Priestley, J. V., & McMahon, S. B. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-08-02651.2001 · Cited by 91 · see citing works
Hains, B. C., Johnson, K. M., McAdoo, D. J., Eaton, M. J., & Hulsebosch, C. E. (2001) · Experimental Neurology · doi:10.1006/exnr.2001.7751 · Cited by 87 · see citing works
Nociceptive pathways: anatomy and physiology of nociceptive ascending pathways
Wd, W. (1985) · Philosophical transactions of the Royal Society of London. Series B, Biological sciences · doi:10.1098/rstb.1985.0025 · Cited by 85 · see citing works
Drew, G. M., Siddall, P. J., & Duggan, A. W. (2001) · Brain Research · doi:10.1016/s0006-8993(00)03288-1 · Cited by 83 · see citing works
Polistina, D. C., Murray, M., & Goldberger, M. E. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.902990307 · Cited by 82 · see citing works
Pierre, J., Mahouche, M., Suderevskaya, E. I., Rep�rant, J., & Ward, R. M. (1997) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19970331)380:1 · Cited by 82 · see citing works
Wallace, C. M., Tator, C. H., & Frazee, P. (1986) · Neurosurgery · doi:10.1227/00006123-198604000-00007 · Cited by 80 · see citing works
Lumbar transplants of immortalized serotonergic neurons alleviate chronic neuropathic pain
Eaton, J. M., Santiago, I. D., Dancausse, A. H., & Whittemore, R. S. (1997) · Pain · doi:10.1016/s0304-3959(97)00015-8 · Cited by 79 · see citing works
Faden, A. I., Gannon, A., & Basbaum, A. I. (1988) · Brain Research · doi:10.1016/0006-8993(88)91548-x · Cited by 78 · see citing works
McNeill, D. L., Carlton, S. M., & Hulsebosch, C. E. (1991) · Experimental Neurology · doi:10.1016/0014-4886(91)90158-9 · Cited by 77 · see citing works
Central inhibitory dysfunctions: Mechanisms and clinical implications
Wiesenfeld‐Hallin, Z., Aldskogius, H., Grant, G., Hao, J.-X., Hökfelt, T., & Xu, X. (1997) · Behavioral and Brain Sciences · doi:10.1017/s0140525x97261480 · Cited by 75 · see citing works
TrkA, trkB, and trkC messenger RNA expression by bulbospinal cells of the rat
King, V. R., Michael, G. J., Joshi, R. K., & Priestley, J. V. (1999) · Neuroscience · doi:10.1016/s0306-4522(99)00072-x · Cited by 70 · see citing works
Effect of intrathecal administration of serotonin in chronic pain models in rats
Bardin, L., Schmidt, J., Alloui, A., & Eschalier, A. (2000) · European Journal of Pharmacology · doi:10.1016/s0014-2999(00)00796-2 · Cited by 67 · see citing works
The Effect of the Sodium Channel Blocker QX-314 on Recovery after Acute Spinal Cord Injury
Agrawal, S., & Fehlings, M. G. (1997) · Journal of Neurotrauma · doi:10.1089/neu.1997.14.81 · Cited by 65 · see citing works
Maiorov, D. N., Fehlings, M. G., & Krassioukov, A. V. (1998) · Journal of Neurotrauma · doi:10.1089/neu.1998.15.365 · Cited by 65 · see citing works
Pitcher, G. M., & Henry, J. L. (2000) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2000.00087.x · Cited by 64 · see citing works
Zhang, B., Goldberger, M. E., & Murray, M. (1993) · Experimental Neurology · doi:10.1006/exnr.1993.1139 · Cited by 60 · see citing works
Garraway, S. M., & Hochman, S. (2001) · Journal of Neurophysiology · doi:10.1152/jn.2001.85.5.1864 · Cited by 59 · see citing works
El-Yassir, N., & Fleetwood-Walker, S. M. (1990) · Brain Research · doi:10.1016/0006-8993(90)91639-x · Cited by 56 · see citing works
Laporte, A., Doyen, C., Nevo, I., Chauveau, J., Hauw, J., & Hamon, M. (1996) · Journal of Chemical Neuroanatomy · doi:10.1016/0891-0618(96)00130-5 · Cited by 56 · see citing works
Li, P., & Zhuo, M. (2001) · Brain Research Bulletin · doi:10.1016/s0361-9230(01)00470-1 · Cited by 55 · see citing works
Identification of 5-hydroxytryptamine1 binding site subtypes in rat spinal cord
Huang, J. C., & Peroutka, S. J. (1987) · Brain Research · doi:10.1016/0006-8993(87)91572-1 · Cited by 53 · see citing works
Robertson, B., Perry, M. J., & Lawson, S. N. (1991) · Journal of Neurocytology · doi:10.1007/bf01355535 · Cited by 52 · see citing works
Long term potentiation of single WDR neurons in spinalized rats
Svendsen, F., Tjølsen, A., Gjerstad, J., & Hole, K. (1999) · Brain Research · doi:10.1016/s0006-8993(98)01250-5 · Cited by 50 · see citing works
Jin, Y., Tessler, A. R., Fischer, I., & Houlé, J. D. (2000) · Neurorehabilitation and neural repair · doi:10.1177/154596830001400407 · Cited by 50 · see citing works
Autonomic dysreflexia in a mouse model of spinal cord injury
Jacob, J. E., Pniak, A., Weaver, L. C., & Brown, A. M. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00436-5 · Cited by 49 · see citing works
Self-citationHao, J., Xu, X., Aldskogius, H., Seiger, Å., & Wiesenfeld‐Hallin, Z. (1992) · Experimental Neurology · doi:10.1016/0014-4886(92)90035-o · Cited by 44 · see citing works
Neurotrophin-3 antisense oligonucleotide attenuates nerve injury-induced Aβ-fibre sprouting
White, D. M. (2000) · Brain Research · doi:10.1016/s0006-8993(00)02940-1 · Cited by 40 · see citing works
Bcl-x L Expression after Contusion to the Rat Spinal Cord
Qiu, J., Nešić, O., Ye, Z., Rea, H., Westlund, K. N., Xu, G.-Y., McAdoo, D. J., Hulsebosch, C. E., & Perez-Polo, J. R. (2001) · Journal of Neurotrauma · doi:10.1089/089771501317095304 · Cited by 39 · see citing works
Hains, B. C., Fullwood, S. D., Eaton, M. J., & Hulsebosch, C. E. (2001) · Brain Research · doi:10.1016/s0006-8993(01)02749-4 · Cited by 37 · see citing works
Sympathetically Correlated Activity of Dorsal Horn Neurons in Spinally Transected Rats
Chau, D. T., Kim, N., & Schramm, L. P. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.77.6.2966 · Cited by 30 · see citing works
Spinal serotonin IA and IC/2 receptors mediate supraspinal μ opioidinduced analgesia
Xu, W., Cui, X., & Han, J. (1994) · Neuroreport · doi:10.1097/00001756-199412000-00065 · Cited by 21 · see citing works
Resection of sciatic nerve re-triggers central sprouting of A-fibre primary afferents in the rat
Ma, Q.-P., Li, T. X., & Woolf, C. J. (2000) · Neuroscience Letters · doi:10.1016/s0304-3940(00)01242-8 · Cited by 12 · see citing works
Çolak, A., Nurlu, G., Açıkgöz, B., Ozcan, O. E., & Aydim, E. (1994) · PubMed · Cited by 1 · see citing works
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Bad news from the brain: descending 5-HT pathways that control spinal pain processing
Suzuki, R., Rygh, L. J., & Dickenson, A. H. (2004) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2004.10.002 · Cited by 483 · see citing works
Chondroitinase ABC Promotes Sprouting of Intact and Injured Spinal Systems after Spinal Cord Injury
Barritt, A. W., Davies, M., Marchand, F., Hartley, R., Grist, J., Yip, P., McMahon, S. B., & Bradbury, E. J. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.2980-06.2006 · Cited by 413 · see citing works
Rat models of spinal cord injury: from pathology to potential therapies
Kjell, J., & Olson, L. (2016) · Disease Models & Mechanisms · doi:10.1242/dmm.025833 · Cited by 408 · see citing works
Karimi‐Abdolrezaee, S., Eftekharpour, E., Wang, J., Schut, D., & Fehlings, M. G. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.3111-09.2010 · Cited by 363 · see citing works
Spinal cord repair strategies: why do they work?
Bradbury, E. J., & McMahon, S. B. (2006) · Nature reviews. Neuroscience · doi:10.1038/nrn1964 · Cited by 352 · see citing works
Gris, D., Marsh, D. R., Oatway, M. A., Chen, Y., Hamilton, E. F., Dekaban, G. A., & Weaver, L. C. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.5343-03.2004 · Cited by 320 · see citing works
Self-citationMechanisms of chronic central neuropathic pain after spinal cord injury
Hulsebosch, C. E., Hains, B. C., Crown, E. D., & Carlton, S. M. (2008) · Brain Research Reviews · doi:10.1016/j.brainresrev.2008.12.010 · Cited by 313 · see citing works
Cannabinoids as Pharmacotherapies for Neuropathic Pain: From the Bench to the Bedside
Rahn, E. J., & Hohmann, A. G. (2009) · Neurotherapeutics · doi:10.1016/j.nurt.2009.08.002 · Cited by 305 · see citing works
Detloff, M. R., Fisher, L. C., McGaughy, V., Longbrake, E. E., Popovich, P. G., & Basso, D. M. (2008) · Experimental Neurology · doi:10.1016/j.expneurol.2008.04.009 · Cited by 278 · see citing works
GABA and central neuropathic pain following spinal cord injury
Gwak, Y. S., & Hulsebosch, C. E. (2011) · Neuropharmacology · doi:10.1016/j.neuropharm.2010.12.030 · Cited by 215 · see citing works
Meisner, J. G., Marsh, A. D., & Marsh, D. R. (2010) · Journal of Neurotrauma · doi:10.1089/neu.2009.1166 · Cited by 198 · see citing works
Neuropathic Pain After Spinal Cord Injury: Challenges and Research Perspectives
Shiao, R., & Lee-Kubli, C. A. (2018) · Neurotherapeutics · doi:10.1007/s13311-018-0633-4 · Cited by 189 · see citing works
Weaver, L. C., Verghese, P. P., Bruce, J. C., Fehlings, M. G., Krenz, N. R., & Marsh, D. R. (2001) · Journal of Neurotrauma · doi:10.1089/08977150152693782 · Cited by 171 · see citing works
Self-citationYousefifard, M., Nasirinezhad, F., Manaheji, H. S., Janzadeh, A., Hosseini, M., & Keshavarz, M. (2016) · Stem Cell Research & Therapy · doi:10.1186/s13287-016-0295-2 · Cited by 146 · see citing works
Rodent models for treatment of spinal cord injury: research trends and progress toward useful repair
Rosenzweig, E. S., & McDonald, J. W. (2004) · Current Opinion in Neurology · doi:10.1097/00019052-200404000-00007 · Cited by 131 · see citing works
The 5-HT3 receptor facilitates at-level mechanical allodynia following spinal cord injury
Oatway, M. A., Chen, Y., & Weaver, L. C. (2004) · Pain · doi:10.1016/j.pain.2004.03.040 · Cited by 125 · see citing works
Self-citationA Graded Forceps Crush Spinal Cord Injury Model in Mice
Plemel, J. R., Duncan, G. J., Chen, K.-W. K., Shannon, C. P., Park, S., Sparling, J. S., & Tetzlaff, W. (2008) · Journal of Neurotrauma · doi:10.1089/neu.2007.0426 · Cited by 122 · see citing works
Neuronal-Glial Interactions Maintain Chronic Neuropathic Pain after Spinal Cord Injury
Gwak, Y. S., Hulsebosch, C. E., & Leem, J. W. (2017) · Neural Plasticity · doi:10.1155/2017/2480689 · Cited by 119 · see citing works
Austin, J. W., Kang, C. E., Baumann, M. D., DiDiodato, L., Satkunendrarajah, K., Wilson, J. R., Stanisz, G. J., Shoichet, M. S., & Fehlings, M. G. (2012) · Biomaterials · doi:10.1016/j.biomaterials.2012.03.022 · Cited by 112 · see citing works
Walters, E. T. (2014) · Experimental Neurology · doi:10.1016/j.expneurol.2014.02.001 · Cited by 106 · see citing works
Wu, Y., Satkunendrarajah, K., Teng, Y., Chow, D. S., Buttigieg, J. A., & Fehlings, M. G. (2013) · Journal of Neurotrauma · doi:10.1089/neu.2012.2622 · Cited by 105 · see citing works
NGF message and protein distribution in the injured rat spinal cord
Brown, A. M., Ricci, M.-J., & Weaver, L. C. (2004) · Experimental Neurology · doi:10.1016/j.expneurol.2004.03.017 · Cited by 105 · see citing works
Self-citationRamer, L. M., Borisoff, J., & Ramer, M. S. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.3337-04.2004 · Cited by 98 · see citing works
Maladaptive spinal plasticity opposes spinal learning and recovery in spinal cord injury
Ferguson, A. R., Huie, J. R., Crown, E. D., Baumbauer, K. M., Hook, M. A., Garraway, S. M., Lee, K. H., Hoy, K. C., & Grau, J. W. (2012) · Frontiers in Physiology · doi:10.3389/fphys.2012.00399 · Cited by 97 · see citing works
Walters, E. T. (2012) · Frontiers in Physiology · doi:10.3389/fphys.2012.00309 · Cited by 92 · see citing works
Mothe, A. J., Tassew, N. G., Shabanzadeh, A. P., Penheiro, R., Vigouroux, R. J., Huang, L., Grinnell, C. M., Cui, Y., Fung, E., Monnier, P. P., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-10987-7 · Cited by 91 · see citing works
Toll-like receptors in central nervous system injury and disease: A focus on the spinal cord
Heiman, A., Pallottie, A., Heary, R. F., & Elkabes, S. (2014) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2014.06.203 · Cited by 91 · see citing works
The dark side of neuroplasticity
Brown, A. M., & Weaver, L. C. (2011) · Experimental Neurology · doi:10.1016/j.expneurol.2011.11.004 · Cited by 90 · see citing works
Self-citationThe Animal Model of Spinal Cord Injury as an Experimental Pain Model
Nakae, A., Nakai, K., Yano, K., Hosokawa, K., Shibata, M., & Mashimo, T. (2011) · BioMed Research International · doi:10.1155/2011/939023 · Cited by 81 · see citing works
Berger, J. V., Knaepen, L., Janssen, S. P. M., Jaken, R. J. P., Marcus, M. A. E., Joosten, E. A. J., & Deumens, R. (2011) · Brain Research Reviews · doi:10.1016/j.brainresrev.2011.03.003 · Cited by 80 · see citing works
Spinal cord injury pain: spinal and supraspinal mechanisms.
Yezierski, R. P. (2009) · PubMed · Cited by 80 · see citing works
Alizadeh, A., Dyck, S. M., Kataria, H., Shahriary, G. M., Nguyen, D. H., Santhosh, K. T., & Karimi‐Abdolrezaee, S. (2017) · Glia · doi:10.1002/glia.23150 · Cited by 78 · see citing works
Oatway, M. A., Chen, Y., Bruce, J. C., Dekaban, G. A., & Weaver, L. C. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.3960-04.2005 · Cited by 77 · see citing works
Self-citationValidity of acute and chronic tactile sensory testing after spinal cord injury in rats
Detloff, M. R., Clark, L. M., Hutchinson, K. J., Kloos, A., Fisher, L. C., & Basso, D. M. (2010) · Experimental Neurology · doi:10.1016/j.expneurol.2010.07.009 · Cited by 73 · see citing works
Due, M. R., Park, J., Zheng, L., Walls, M. K., Allette, Y. M., White, F. A., & Shi, R. (2013) · Journal of Neurochemistry · doi:10.1111/jnc.12500 · Cited by 69 · see citing works
Ditor, D. S., John, S. M., Roy, J., Marx, J. C., Kittmer, C., & Weaver, L. C. (2007) · Journal of Neuroscience Research · doi:10.1002/jnr.21283 · Cited by 67 · see citing works
Self-citationWebb, A. A., Gowribai, K., & Muir, G. D. (2003) · Behavioural Brain Research · doi:10.1016/s0166-4328(03)00076-7 · Cited by 67 · see citing works
Dugan, E. A., Jergová, S., & Sagen, J. (2020) · Experimental Neurology · doi:10.1016/j.expneurol.2020.113208 · Cited by 64 · see citing works
Regional Hyperexcitability and Chronic Neuropathic Pain Following Spinal Cord Injury
Kang, J., Cho, S. S., Kim, H. Y., Lee, B. H., Cho, H. J., & Gwak, Y. S. (2020) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-020-00785-7 · Cited by 64 · see citing works
Hoschouer, E. L., Basso, M. D., & Jakeman, L. B. (2009) · Pain · doi:10.1016/j.pain.2009.11.023 · Cited by 58 · see citing works
Effect of Age at Time of Spinal Cord Injury on Behavioral Outcomes in Rat
Gwak, Y. S., Hains, B. C., Johnson, K. M., & Hulsebosch, C. E. (2004) · Journal of Neurotrauma · doi:10.1089/0897715041650999 · Cited by 58 · see citing works
Antinociceptive Effect of Riluzole in Rats with Neuropathic Spinal Cord Injury Pain
Hama, A. T., & Sagen, J. (2010) · Journal of Neurotrauma · doi:10.1089/neu.2010.1539 · Cited by 57 · see citing works
Hama, A. T., & Sagen, J. (2007) · Brain Research · doi:10.1016/j.brainres.2007.09.013 · Cited by 57 · see citing works
Hama, A. T., & Sagen, J. (2011) · Brain Research · doi:10.1016/j.brainres.2011.07.031 · Cited by 56 · see citing works
Donovan-Rodríguez, T., Urch, C., & Dickenson, A. H. (2005) · Neuroscience Letters · doi:10.1016/j.neulet.2005.09.073 · Cited by 54 · see citing works
Hu, Y. S., Wen, C.-Y., Li, T.-H., Cheung, M. M., Wu, E. X., & Luk, K. D. K. (2011) · Clinical Neurophysiology · doi:10.1016/j.clinph.2010.12.051 · Cited by 52 · see citing works
Weaver, L. C., Gris, D., Saville, L. R., Oatway, M. A., Chen, Y., Marsh, D. R., Hamilton, E. F., & Dekaban, G. A. (2005) · Journal of Neurotrauma · doi:10.1089/neu.2005.22.1375 · Cited by 52 · see citing works
Self-citationPain behaviors after spinal cord contusion injury in two commonly used mouse strains
Kerr, B. J., & David, S. (2007) · Experimental Neurology · doi:10.1016/j.expneurol.2007.04.014 · Cited by 50 · see citing works
Bilateral Contusion-Compression Model of Incomplete Traumatic Cervical Spinal Cord Injury
Forgione, N., Karadimas, S. K., Foltz, W. D., Satkunendrarajah, K., Lip, A., & Fehlings, M. G. (2014) · Journal of Neurotrauma · doi:10.1089/neu.2014.3388 · Cited by 49 · see citing works
Dugan, E. A., & Sagen, J. (2014) · Journal of Neurotrauma · doi:10.1089/neu.2014.3692 · Cited by 46 · see citing works
Immunocytochemical localization of TNF type 1 and type 2 receptors in the rat spinal cord
Holmes, G. M., Hebert, S. L., Rogers, R. C., & Hermann, G. E. (2004) · Brain Research · doi:10.1016/j.brainres.2004.08.020 · Cited by 46 · see citing works
Colpaert, F. C., Wu, W.-P., Hao, J., Royer, I., Sautel, F., Wiesenfeld‐Hallin, Z., & Xu, X. (2004) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2004.06.026 · Cited by 45 · see citing works
Densmore, V. S., Kalous, A., Keast, J. R., & Osborne, P. B. (2010) · Pain · doi:10.1016/j.pain.2010.07.007 · Cited by 44 · see citing works
Mothe, A. J., Coelho, M. P., Huang, L., Monnier, P. P., Cui, Y., Mueller, B. K., Jacobson, P. B., & Tator, C. H. (2020) · Neurobiology of Disease · doi:10.1016/j.nbd.2020.104995 · Cited by 43 · see citing works
Effects of Pain and Pain Management on Motor Recovery of Spinal Cord–Injured Patients
Cragg, J. J., Haefeli, J., Jutzeler, C. R., Röhrich, F., Weidner, N., Saur, M., Maier, D. D., Kalke, Y.-B., Schuld, C., Curt, A. E. P., et al. (2016) · Neurorehabilitation and neural repair · doi:10.1177/1545968315624777 · Cited by 43 · see citing works
Frailty and pain, human studies and animal models
D’Agnelli, S., Amodeo, G., Franchi, S., Verduci, B., Baciarello, M., Panerai, A. E., Bignami, E. G., & Sacerdote, P. (2021) · Ageing Research Reviews · doi:10.1016/j.arr.2021.101515 · Cited by 42 · see citing works
Antinociceptive effect of cannabinoid agonist WIN 55,212-2 in rats with a spinal cord injury
Hama, A., & Sagen, J. (2007) · Experimental Neurology · doi:10.1016/j.expneurol.2006.09.002 · Cited by 40 · see citing works
Crown, E. D. (2011) · Experimental Neurology · doi:10.1016/j.expneurol.2011.10.019 · Cited by 40 · see citing works
Chen, Y., Oatway, M. A., & Weaver, L. C. (2008) · Journal of Neuroscience Research · doi:10.1002/jnr.21860 · Cited by 39 · see citing works
Self-citationYamazaki, K., Kawabori, M., Seki, T., Takamiya, S., Tateno, T., Konno, K., Watanabe, M., & Houkin, K. (2020) · Journal of Neurotrauma · doi:10.1089/neu.2019.6905 · Cited by 38 · see citing works
Lee, J., Choi, C., Chung, D., Kang, E., Chang, H.-S., Hwang, S., Han, H. J., Choe, B., Sur, J., Lee, S., et al. (2007) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2007.07.020 · Cited by 38 · see citing works
Experimental spinal cord trauma: a review of mechanically induced spinal cord injury in rat models
Abdullahi, D., Ahmad‐Annuar, A., Mohamad, M., Aziz, I., & Sanusi, J. (2016) · Reviews in the Neurosciences · doi:10.1515/revneuro-2016-0050 · Cited by 37 · see citing works
Walters, E. T. (2017) · Autonomic Neuroscience · doi:10.1016/j.autneu.2017.01.006 · Cited by 37 · see citing works
Huang, Y.-J., & Grau, J. W. (2018) · Experimental Neurology · doi:10.1016/j.expneurol.2018.05.002 · Cited by 36 · see citing works
Figley, S. A., Liu, Y., Karadimas, S. K., Satkunendrarajah, K., Fettes, P., Spratt, S. K., Lee, G., Ando, D. G., Surosky, R. T., Giedlin, M. A., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0096137 · Cited by 33 · see citing works
The gut-brain axis and beyond: Microbiome control of spinal cord injury pain in humans and rodents
Bannerman, C. A., Douchant, K., Sheth, P. M., & Ghasemlou, N. (2020) · Neurobiology of Pain · doi:10.1016/j.ynpai.2020.100059 · Cited by 33 · see citing works
Kalous, A., Osborne, P. B., & Keast, J. R. (2007) · The Journal of Comparative Neurology · doi:10.1002/cne.21412 · Cited by 33 · see citing works
Coderre, T. J., & Laferrière, A. (2019) · Journal of Neural Transmission · doi:10.1007/s00702-019-02103-y · Cited by 32 · see citing works
Hama, A. T., Broadhead, A. R., Lorrain, D. S., & Sagen, J. (2011) · Journal of Neurotrauma · doi:10.1089/neu.2011.1863 · Cited by 31 · see citing works
Gris, D., Marsh, D. R., Dekaban, G. A., & Weaver, L. C. (2005) · Experimental Neurology · doi:10.1016/j.expneurol.2005.03.016 · Cited by 31 · see citing works
Self-citationHama, A. T., & Sagen, J. (2012) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2012.03.015 · Cited by 31 · see citing works
Tibbett, J. A., Field-Fote, E. C., Thomas, C. K., & Widerström-Noga, E. G. (2019) · PM&R · doi:10.1002/pmrj.12218 · Cited by 29 · see citing works
Fauss, G. N. K., Hudson, K. E., & Grau, J. W. (2022) · Biology · doi:10.3390/biology11020234 · Cited by 29 · see citing works
SPINAL CORD INJURY: CURRENT MAMMALIAN MODELS
Kundi, S. (2013) · Neuroscience International · doi:10.3844/amjnsp.2013.1.12 · Cited by 29 · see citing works
Kalous, A., Osborne, P. B., & Keast, J. R. (2009) · The Journal of Comparative Neurology · doi:10.1002/cne.21986 · Cited by 29 · see citing works
Yamazaki, K., Kawabori, M., Seki, T., Takamiya, S., Konno, K., Watanabe, M., Houkin, K., & Fujimura, M. (2021) · Stem Cells International · doi:10.1155/2021/9964877 · Cited by 28 · see citing works
Hajimashhadi, Z., Aboutaleb, N., & Nasirinezhad, F. (2016) · Neuropeptides · doi:10.1016/j.npep.2016.08.010 · Cited by 26 · see citing works
Eeswara, A., Pacheco-Spiewak, A., Jergová, S., & Sagen, J. (2023) · PLoS ONE · doi:10.1371/journal.pone.0282920 · Cited by 26 · see citing works
Robins, S. L., Nguyen, D. H., & Fehlings, M. G. (2012) · Journal of Neurotrauma · doi:10.1089/neu.2011.2005 · Cited by 22 · see citing works
Dugan, E. A., Schachner, B. I., Jergová, S., & Sagen, J. (2020) · Journal of Neurotrauma · doi:10.1089/neu.2020.7378 · Cited by 22 · see citing works
Ditor, D. S., John, S. M., Cakiroglu, J., Kittmer, C., Foster, P. J., & Weaver, L. C. (2008) · Journal of Neurosurgery Spine · doi:10.3171/spi/2008/9/9/301 · Cited by 21 · see citing works
Self-citationEaton, M. J., & Wolfe, S. Q. (2009) · PubMed · Cited by 19 · see citing works
Restorative effects of stimulating medullary raphe after spinal cord injury.
Hentall, I. D., & Burns, S. (2009) · PubMed · Cited by 19 · see citing works
Suppression of microglial Ccl2 reduces neuropathic pain associated with chronic spinal compression
Li, Q., Yang, Z., Wang, K., Chen, Z., & Shen, H. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1191188 · Cited by 17 · see citing works
Eaton, M. J., Widerström-Noga, E. G., & Wolfe, S. Q. (2011) · Neurology Research International · doi:10.1155/2011/891605 · Cited by 16 · see citing works
Lee, J. W., Jergová, S., Furmanski, O., Gajavelli, S., & Sagen, J. (2012) · Frontiers in Physiology · doi:10.3389/fphys.2012.00167 · Cited by 16 · see citing works
Neuropathic Pain Induced by Spinal Cord Injury from the Glia Perspective and Its Treatment
Ying, Y., Su, X., Tang, J., & Zhu, C. (2024) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-024-01517-x · Cited by 15 · see citing works
XIE, Y.-G., MU, H.-J., Li, Z., Ma, J., & Wang, Y. (2014) · Experimental and Therapeutic Medicine · doi:10.3892/etm.2014.1878 · Cited by 15 · see citing works
Prolonged nociceptive responses to hind paw formalin injection in rats with a spinal cord injury
Lee, J. W., Furmanski, O., Castellanos, D. A., Daniels, L. A., Hama, A. T., & Sagen, J. (2008) · Neuroscience Letters · doi:10.1016/j.neulet.2008.05.030 · Cited by 15 · see citing works
Chapter 14 Descending excitatory systems
Ossipov, M. H., & Porreca, F. (2006) · Handbook of clinical neurology · doi:10.1016/s0072-9752(06)80018-7 · Cited by 13 · see citing works
On-ong-arj, P., Wattanathorn, J., Muchimapura, S., & Thukham-mee, W. (2018) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2018/5407052 · Cited by 13 · see citing works
Jergová, S., Gordon, C. E., Gajavelli, S., & Sagen, J. (2017) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2017.00406 · Cited by 13 · see citing works
Carter, M. W., Johnson, K. M., Lee, J. Y., Hulsebosch, C. E., & Gwak, Y. S. (2016) · The Korean journal of pain · doi:10.3344/kjp.2016.29.2.86 · Cited by 13 · see citing works
Yasko, J. R., Moss, I. L., & Mains, R. E. (2019) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2019.00284 · Cited by 12 · see citing works
Oudega, M., Chao, O. Y.-H., Avison, D. L., Bronson, R. T., Buchser, W., Hurtado, A., & Grimpe, B. (2012) · Experimental Neurology · doi:10.1016/j.expneurol.2012.06.006 · Cited by 12 · see citing works
Diffusion tensor imaging of the spinal cord: a review
Vedantam, A., Jirjis, M. B., Eckhardt, G., Sharma, A., Schmit, B. D., Wang, M. C., Ulmer, J. L., & Kurpad, S. N. (2013) · Coluna/Columna · doi:10.1590/s1808-18512013000100014 · Cited by 12 · see citing works
Spinal Cord Mechanisms of Hyperalgesia and Allodynia
Coderre, T. J. (2008) · Elsevier eBooks · doi:10.1016/b978-012370880-9.00168-7 · Cited by 11 · see citing works
Sex differences in effects of excitotoxic spinal injury on below-level pain sensitivity
Acosta-Rua, A. J., Cannon, R. L., Yezierski, R. P., & Vierck, C. J. (2011) · Brain Research · doi:10.1016/j.brainres.2011.08.072 · Cited by 11 · see citing works
Lee, H. J., Malone, P. S., Chung, J., White, J. M., Wilson, N., Tidwell, J., & Tansey, K. E. (2019) · Neural Plasticity · doi:10.1155/2019/6147878 · Cited by 11 · see citing works
Spinal cord injury in mice affects central and peripheral pathology in a severity-dependent manner
Bannerman, C. A., Douchant, K., Segal, J. P., Knezic, M., Mack, A. E., Lundell-Creagh, C., Silva, J. R., Duggan, S., Sheth, P. M., & Ghasemlou, N. (2021) · Pain · doi:10.1097/j.pain.0000000000002471 · Cited by 10 · see citing works
- Authors
- Bruce, J. C., Oatway, M. A., & Weaver, L. C.
- Affiliations
- Robarts Research Institute (CA)
- Corresponding author
- Weaver, Lynne C.
- Venue
- Experimental Neurology
- Publisher
- Elsevier BV
- Published
- 2002-11
- Volume
- 178
- Issue
- 1
- Pages
- 33-48
- ISSN
- 0014-4886 (ISSN-L)
- OpenAlex
- W2021904427
- Cited by
- 137
- References
- 68
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 1 · 2023: 4 · 2022: 1 · 2021: 5 · 2020: 8 · 2019: 6 · 2018: 6 · 2017: 5 · 2016: 6 · 2015: 2 · 2014: 7 · 2013: 10 · 2012: 8
- FWCI
- 3.80
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Experimental Neurology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Heart and Stroke Foundation of Canada
- Snap
- Ontario Neurotrauma Foundation
- Topics
- Health Sciences › Medicine › Physiology › Pain Mechanisms and Treatments
- Health Sciences › Medicine › Pathology and Forensic Medicine › Spinal Cord Injury Research
- Health Sciences › Medicine › Anesthesiology and Pain Medicine › Pain Management and Treatment
- Keywords
- chronic pain, spinal cord injury, clip compression injury, mechanical allodynia, hyperalgesia, primary sensory neurons, serotonin, descending serotonergic pathways, dorsal horn, pronociception, thoracic spinal cord
- MeSH terms
- Animals, Chronic Disease, Disease Models, Animal, Hyperalgesia, Male, Motor Activity, Nerve Fibers, Myelinated, Neural Inhibition, Neuronal Plasticity, Neurons, Afferent, Pain, Serotonin, Spinal Cord, Spinal Cord Compression, Surgical Instruments, Touch, Rats, Wistar, Nerve Fibers, Unmyelinated, Rats
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