The DOI matches its Crossref record; 57 of the 57 references it cites were found in a registry or an index.
Adrenergic innervation of rat sensory ganglia following proximal or distal painful sciatic neuropathy: distinct mechanisms revealed by anti‐NGF treatment
Abstract
Sympathetic axons invade dorsal root ganglia (DRG) following nerve injury, and activity in the resulting pericellular axonal ‘baskets’ may underlie painful sympathetic–sensory coupling. Sympathetic sprouting into the DRG may be stimulated by nerve growth factor (NGF). To test this hypothesis, we investigated the effect of daily anti‐NGF administration on pain and on sprouting in the DRG induced by chronic sciatic constriction injury (CCI) or L5 spinal nerve ligation (SNL). These models have been shown to differ subtly in the onset of pain behaviours and adrenergic sprouting, and we now demonstrate a fundamental difference in the way sympathetic axons invade the DRG: after CCI, perivascular noradrenergic collaterals sprouted into the DRG in a manner dependent upon peripherally derived NGF. In contrast, after SNL, regenerating sympathetic axons were diverted towards the DRG from the spinal nerve by the obstructing ligature, and this effect was only moderately impeded by anti‐NGF. The differential dependence on anti‐NGF suggests that adrenergic innervation of the DRG after SNL and CCI may reflect regenerative and collateral sprouting, respectively. Pain behaviour was similarly affected: anti‐NGF completely prevented CCI‐induced thermal hyperalgesia and mechanoallodynia, but the same treatment only partly relieved these symptoms following SNL. These differences emphasize that although CCI and SNL may result in similar behavioural abnormalities, the underlying mechanisms may be governed by distinct processes, differentially dependent on peripheral NGF. These mechanistic differences will have to be considered in the development of appropriate treatment strategies for neuropathic pain produced by different types of pathology.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“Lesions may produce pain by compressing or infiltrating nerves near lesions”
From Chronic pelvic pain and endometriosis: translational evidence of the relationship and implications (2011) · cites this paper as Ramer and Bisby, 1999
Citations
Cites
Ethical guidelines for investigations of experimental pain in conscious animals.
Zimmermann, M. (1983) · Pain · doi:10.1016/0304-3959(83)90201-4 · Cited by 7,762
A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man
Bennett, G. J., & Xie, Y.-K. (1988) · Pain · doi:10.1016/0304-3959(88)90209-6 · Cited by 5,376
A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia
Hargreaves, K., Dubner, R. A., Brown, F. J., Flores, C., & Joris, J. L. (1988) · Pain · doi:10.1016/0304-3959(88)90026-7 · Cited by 5,155
Ho Kim, S., & Mo Chung, J. (1992) · Pain · doi:10.1016/0304-3959(92)90041-9 · Cited by 3,069
Heumann, R., Korsching, S. I., Bandtlow, C. E., & Thoenen, H. (1987) · The Journal of Cell Biology · doi:10.1083/jcb.104.6.1623 · Cited by 1,022
Peripheral nerve injury triggers noradrenergic sprouting within dorsal root ganglia
McLachlan, E. M., Jänig, W., Devor, M. G., & Michaelis, M. (1993) · Nature · doi:10.1038/363543a0 · Cited by 739
Nerve growth factor-induced hyperalgesia in the neonatal and adult rat
Lewin, G. R., Ritter, A., & Mendell, L. M. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-05-02136.1993 · Cited by 562
McMahon, S. B., Bennett, D., Priestley, J. V., & Shelton, D. L. (1995) · Nature Medicine · doi:10.1038/nm0895-774 · Cited by 435
Comparison of three rodent neuropathic pain models
Kim, K. J., & Chung, J. M. (1997) · Experimental Brain Research · doi:10.1007/bf02450318 · Cited by 419
Verge, V., Merlio, J., Grondin, J., Ernfors, P., Persson, H., Rj, R., Hökfelt, T. G. M., & Richardson, P. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-10-04011.1992 · Cited by 339
NGF as a mediator of inflammatory pain
McMahon, S. B. (1996) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.1996.0039 · Cited by 332
Brown, M. C., Perry, V. H., Lunn, E. R., Gordon, S., & Heumann, R. (1991) · Neuron · doi:10.1016/0896-6273(91)90245-u · Cited by 307
Wright, D. E., & Snider, W. D. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903510302 · Cited by 303
Devor, M. G., Jänig, W., & Michaelis, M. (1994) · Journal of Neurophysiology · doi:10.1152/jn.1994.71.1.38 · Cited by 269
Jänig, W., Levine, J. D., & Michaelis, M. (1996) · Progress in brain research · doi:10.1016/s0079-6123(08)61087-0 · Cited by 260
The spectrum of fiber loss in a model of neuropathic pain in the rat: an electron microscopic study
Basbaum, A. I., Gautron, M., Jazat, F., Mayes, M., & Guilbaud, G. (1991) · Pain · doi:10.1016/0304-3959(91)90229-q · Cited by 252
Peripheral cell types contributing to the hyperalgesic action of nerve growth factor in inflammation
Woolf, C. J., Ma, Q., Allchorne, A. J., & Poole, S. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-08-02716.1996 · Cited by 236
Human mast cells express functional TrkA and are a source of nerve growth factor
Nilsson, G. P., Forsberg‐Nilsson, K., Xiang, Z., Hallböök, F., Nilsson, K., & Metcalfe, D. D. (1997) · European Journal of Immunology · doi:10.1002/eji.1830270925 · Cited by 210
Functional changes in dorsal root ganglion cells after chronic nerve constriction in the rat
Xie, Y., Zhang, J., Petersen, M., & LaMotte, R. H. (1995) · Journal of Neurophysiology · doi:10.1152/jn.1995.73.5.1811 · Cited by 190
Diamond, J., Foerster, A. F., Holmes, M., & Coughlin, M. D. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-04-01467.1992 · Cited by 189
Ramer, M., Murphy, P. G., Richardson, P., & Bisby, M. A. (1998) · Pain · doi:10.1016/s0304-3959(98)00121-3 · Cited by 175
Self-citationSebert, M. E., & Shooter, E. M. (1993) · Journal of Neuroscience Research · doi:10.1002/jnr.490360402 · Cited by 173
Toledo‐Aral, J. J., Brehm, P., Halegoua, S., & Mandel, G. (1995) · Neuron · doi:10.1016/0896-6273(95)90317-8 · Cited by 167
The union of different kinds of nerve fibres
Langley, J. N., & Anderson, H. K. (1904) · The Journal of Physiology · doi:10.1113/jphysiol.1904.sp001042 · Cited by 166
Wallerian degeneration is required for both neuropathic pain and sympathetic sprouting into the DRG
Ramer, M. S., French, G. D., & Bisby, M. A. (1997) · Pain · doi:10.1016/s0304-3959(97)00019-5 · Cited by 162
Self-citationChung, K., Kim, H. J., Na, H. S., Park, M. J., & Chung, J. M. (1993) · Neuroscience Letters · doi:10.1016/0304-3940(93)90566-4 · Cited by 162
NGF involvement in pain induced by chronic constriction injury of the rat sciatic nerve
Herzberg, U., Eliav, E., Dorsey, J. M., Gracely, R. H., & Kopin, I. J. (1997) · Neuroreport · doi:10.1097/00001756-199705060-00012 · Cited by 153
Ramer, M. S., & Bisby, M. A. (1997) · Pain · doi:10.1016/s0304-3959(97)03331-9 · Cited by 152
Self-citationThe Neurosciences: Paths of Discovery
McHenry, L. C. (1976) · JAMA · doi:10.1001/jama.1976.03270080059039 · Cited by 140
Pathology of Experimental Compression Neuropathy Producing Hyperesthesia
Sommer, C., Galbraith, J. A., Heckman, H. M., & Myers, R. R. (1993) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/00005072-199305000-00006 · Cited by 135
Adrenoreceptor subtype mediating sympathetic-sensory coupling in injured sensory neurons
Chen, Y., Michaelis, M., Jänig, W., & Devor, M. G. (1996) · Journal of Neurophysiology · doi:10.1152/jn.1996.76.6.3721 · Cited by 132
Increased NGF mRNA expression in denervated rat skin
Mearow, K. M., Kril, Y., & Diamond, J. (1993) · Neuroreport · doi:10.1097/00001756-199304000-00002 · Cited by 111
de la Torre, J. C. (1980) · Neuroscience Letters · doi:10.1016/0304-3940(80)90047-6 · Cited by 109
Neil, A., Attal, N., & Guilbaud, G. (1991) · Brain Research · doi:10.1016/0006-8993(91)91655-k · Cited by 101
Davis, B. M., Albers, K. M., Seroogy, K. B., & Katz, D. M. (1994) · The Journal of Comparative Neurology · doi:10.1002/cne.903490310 · Cited by 96
Gloster, A. T., & Diamond, J. (1992) · The Journal of Comparative Neurology · doi:10.1002/cne.903260305 · Cited by 91
Michaelis, M., Devor, M. G., & Jänig, W. (1996) · Journal of Neurophysiology · doi:10.1152/jn.1996.76.2.753 · Cited by 89
Local injection of nerve growth factor (NGF) triggers degranulation of mast cells in rat paw
Tal, M., & Liberman, R. (1997) · Neuroscience Letters · doi:10.1016/s0304-3940(96)13318-8 · Cited by 80
Morphological properties of intracellularly labeled layer I neurons in rat neocortex
Zhou, F.-M., & Hablitz, J. J. (1996) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19961209)376:2 · Cited by 79
Agius, E., & Cochard, P. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-01-00328.1998 · Cited by 78
Chung, K., Yoon, Y. W., & Chung, J. M. (1997) · Brain Research · doi:10.1016/s0006-8993(96)01408-4 · Cited by 78
Amann, R., SIRINATHSINGHJI, D. J. S., Donnerer, J., Liebmann, I., & Schuligoi, R. (1996) · Neuroscience Letters · doi:10.1016/0304-3940(95)12287-7 · Cited by 76
Nerve growth factor alleviates a painful peripheral neuropathy in rats
Ren, K., Thomas, D. A., & Dubner, R. A. (1995) · Brain Research · doi:10.1016/0006-8993(95)00920-l · Cited by 69
Interleukin‐2 enhances chick and rat sympathetic, but not sensory, neurite outgrowth
Haugen, P., & Letourneau, P. C. (1990) · Journal of Neuroscience Research · doi:10.1002/jnr.490250402 · Cited by 67
Desmeules, J. A., Kayser, V., Weil-Fuggaza, J., Aubel, B., & Guilbaud, G. (1995) · Neuroscience · doi:10.1016/0306-4522(95)00098-4 · Cited by 67
Poor Growth of Mammalian Motor and Sensory Axons Into Intact Proximal Nerve Stumps
Brown, M. C., Lunn, E. R., & Perry, V. H. (1991) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1991.tb00069.x · Cited by 45
Differences in Sympathetic Innervation of Mouse DRG Following Proximal or Distal Nerve Lesions
Ramer, M. S., & Bisby, M. A. (1998) · Experimental Neurology · doi:10.1006/exnr.1998.6855 · Cited by 44
Self-citationHendry, I. A. (1973) · Brain Research · doi:10.1016/0006-8993(73)90344-2 · Cited by 44
Ramer, M. S., & Bisby, M. A. (1997) · Neuroscience Letters · doi:10.1016/s0304-3940(97)00356-x · Cited by 43
Self-citationWells, M. R., Vaidya, U., & Schwartz, J. P. (1994) · Experimental Brain Research · doi:10.1007/bf00243216 · Cited by 39
Mathew, T. C., & Miller, F. D. (1993) · Developmental Biology · doi:10.1006/dbio.1993.1204 · Cited by 31
Ro, L., Chen, S.-T., Tang, L., & Chang, H. (1996) · Neuroscience Letters · doi:10.1016/s0304-3940(96)13109-8 · Cited by 25
Neurotrophin Sensitivity of Prevertebral and Paravertebral Rat Sympathetic Autonomic Ganglia
Schmidt, R. E., Dorsey, D. A., Selznick, L. A., DiStefano, P. S., Carroll, S. L., Beaudet, L. N., & Roth, K. A. (1998) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/00005072-199802000-00007 · Cited by 20
Pretreatment with Interleukin-1 Enhances Survival of Sympathetic Ganglionic Neuron Grafts
Nakao, N., Itakura, T., Uematsu, Y., Nakai, M., Komai, N., & Furukawa, S. (1994) · Neurologia medico-chirurgica · doi:10.2176/nmc.34.407 · Cited by 15
SOMATIC VERSUS SYMPATHETIC MEDIATED CHRONIC LIMB PAIN
Cooney, W. P. (1997) · Hand Clinics · doi:10.1016/s0749-0712(21)00096-2 · Cited by 13
Association of basal lamina with peripheral axons elongating within the rat central nervous system
Crutcher, K. A., & Chandler, J. P. (1984) · Brain Research · doi:10.1016/0006-8993(84)90933-8 · Cited by 11
SOMATIC OR SYMPATHETIC BLOCK FOR REFLEX SYMPATHETIC DYSTROPHY
Brown, D. L. (1997) · Hand Clinics · doi:10.1016/s0749-0712(21)00107-4 · Cited by 10
Research works printed but not linked: 3
- Jänig W., 1991, Towards a New Pharmacotherapy of Pain., 331
- Ramer M.S., 1995, Neuropathic pain and sympathetic sprouting in the dorsal root ganglion: the effect of partial nerve injury and NGF. Soc., Neurosci. Abstract., 22, 1809
- Thompson S.W.N., 1997, Leukemia inhibitory factor (LIF) induces sympathetic sprouting and pericellular basket formation in intact adult rat sensory ganglia. Soc., Neurosci. Abstract., 23, 1432
Cited by
Sorted by citations
Tanezumab for the Treatment of Pain from Osteoarthritis of the Knee
Lane, N. E., Schnitzer, T. J., Birbara, C. A., Mokhtarani, M., Shelton, D. L., Smith, M. D., & Brown, M. (2010) · New England Journal of Medicine · doi:10.1056/nejmoa0901510 · Cited by 685
Austin, P. J., & Moalem-Taylor, G. (2010) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2010.08.013 · Cited by 607
Chronic pelvic pain and endometriosis: translational evidence of the relationship and implications
Stratton, P., & Berkley, K. J. (2011) · Human Reproduction Update · doi:10.1093/humupd/dmq050 · Cited by 442
Novel class of pain drugs based on antagonism of NGF
Hefti, F. F., Rosenthal, A., Walicke, P. A., Wyatt, S. L., Vergara, G., Shelton, D. L., & Davies, A. M. (2005) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2005.12.001 · Cited by 380
Topical and Peripherally Acting Analgesics
Sawynok, J. (2003) · Pharmacological Reviews · doi:10.1124/pr.55.1.1 · Cited by 347
Metadata
- Authors
- Ramer, M. S., & Bisby, M. A.
- Affiliations
- Queen's University (CA)
- Corresponding author
- Ramer, Matt S.
- ORCID
- Bisby, Mark A.
- Venue
- European Journal of Neuroscience
- Publisher
- Wiley
- Published
- 1999-03
- Volume
- 11
- Issue
- 3
- Pages
- 837-846
- ISSN
- 0953-816X (ISSN-L)
- 1460-9568
- OpenAlex
- W1985937673
- Cited by
- 116
- References
- 57
- Citations by year
- 2026: 2 · 2025: 1 · 2024: 1 · 2023: 2 · 2022: 1 · 2021: 2 · 2020: 5 · 2019: 1 · 2018: 2 · 2017: 2 · 2016: 5 · 2015: 3 · 2014: 6 · 2013: 4 · 2012: 3
- FWCI
- 3.54
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- European Journal of Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Physiology (medical) › Pain Mechanisms and Treatments
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Nerve injury and regeneration
- Health Sciences › Medicine › Anesthesiology and Pain Medicine › Pain Management and Treatment
- Keywords
- adrenergic innervation, dorsal root ganglia, nerve growth factor, spinal nerve ligation, painful neuropathy, thermal hyperalgesia
- MeSH terms
- Adrenergic Fibers, Animals, Antibodies, Behavior, Animal, Ganglia, Spinal, Ligation, Male, Nerve Growth Factors, Nerve Regeneration, Neurons, Afferent, Pain, Receptors, Adrenergic, Sciatic Nerve, Sciatica, Sympathectomy, Wallerian Degeneration, Rats, Sprague-Dawley, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review