The DOI matches its Crossref record; 47 of the 47 references it cites were found in a registry or an index.
Neuromuscular activity impairs axonal sprouting in partially denervated muscles by inhibiting bridge formation of perisynaptic Schwann cells
Abstract
Following partial denervation of rat hindlimb muscle, terminal Schwann cells extend processes from denervated endplates to induce and guide sprouting from the remaining intact axons. Increased neuromuscular activity significantly reduces motor unit enlargement and sprouting during the acute phase of sprouting. These findings led to the hypothesis that increased neuromuscular activity perturbs formation of Schwann cell bridges and thereby reduces sprouting. Adult rat tibialis anterior (TA) muscles were extensively denervated by avulsion of L4 spinal root and were immediately subjected to normal caged activity or running exercise (8 h daily) for 3, 7, 14, 21, and 28 days. Combined silver/cholinesterase histochemical staining revealed that the progressive reinnervation of denervated endplates by sprouts over a 1 month period in the extensively partially denervated TA muscles was completely abolished by increased neuromuscular activity. Immunohistochemical staining and triple immunofluorescence revealed that the increased neuromuscular activity did not perturb the production of Schwann cell processes, but prevented bridging between Schwann cell processes at innervated and denervated endplates. Our findings suggest that failure of Schwann cell processes to bridge between endplates accounts, at least in part, for the inhibitory effect of increased neuromuscular activity on sprouting. © 2003 Wiley Periodicals, Inc. J Neurobiol 57: 221–234, 2003
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?
Collateral sprouting in motor nerves and regeneration in sensory nerves are modulated by the neural activity.
“Collateral sprouting in motor nerves and regeneration in sensory nerves are modulated by the neural activity [107–110].”
From Safety of long-term electrical peripheral nerve stimulation: review of the state of the art (2019) · cites this paper as [109]
Citations
Cites
Regulation of growth cone behavior by calcium
Kater, S. B., & Mills, L. (1991) · Journal of Neuroscience · doi:10.1523/jneurosci.11-04-00891.1991 · Cited by 595
Calcium regulation of the neuronal growth cone
Kater, S. B., Mattson, M. P., Cohan, C. S., & Connor, J. A. (1988) · Trends in Neurosciences · doi:10.1016/0166-2236(88)90094-x · Cited by 579
Brown, M. C., Holland, R. L., & Hopkins, W. G. (1981) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.04.030181.000313 · Cited by 528
Caroni, P., & Grandes, P. (1990) · The Journal of Cell Biology · doi:10.1083/jcb.110.4.1307 · Cited by 441
Calcium regulation of neurite elongation and growth cone motility
Mattson, M. P., & Kater, S. B. (1987) · Journal of Neuroscience · doi:10.1523/jneurosci.07-12-04034.1987 · Cited by 421
The Neurobiology of Depression
Nemeroff, C. B. (1998) · Scientific American · doi:10.1038/scientificamerican0698-42 · Cited by 381
Sprouting and regression of neuromuscular synapses in partially denervated mammalian muscles.
Brown, M. C., & Ironton, R. (1978) · The Journal of Physiology · doi:10.1113/jphysiol.1978.sp012307 · Cited by 314
Nerve sprouting in muscle is induced and guided by processes extended by schwann cells
Son, Y., & Thompson, W. J. (1995) · Neuron · doi:10.1016/0896-6273(95)90247-3 · Cited by 312
Electrically and chemically mediated increases in intracellular calcium in neuronal growth cones
Cohan, C. S., Connor, J. A., & Kater, S. B. (1987) · Journal of Neuroscience · doi:10.1523/jneurosci.07-11-03588.1987 · Cited by 286
Thompson, W. J., & Jansen, J. K. S. (1977) · Neuroscience · doi:10.1016/0306-4522(77)90049-5 · Cited by 256
Schwann cells induce and guide sprouting and reinnervation of neuromuscular junctions
Son, Y., Trachtenberg, J. T., & Thompson, W. J. (1996) · Trends in Neurosciences · doi:10.1016/s0166-2236(96)10032-1 · Cited by 241
Transmitter release increases intracellular calcium in perisynaptic schwann cells in situ
Jahromi, B. S., Robitaille, R., & Charlton, M. P. (1992) · Neuron · doi:10.1016/0896-6273(92)90128-z · Cited by 229
Thesleff, S. (1976) · Medical Entomology and Zoology · Cited by 217
Terminal Schwann cells elaborate extensive processes following denervation of the motor endplate
Reynolds, M. L., & Woolf, C. J. (1992) · Journal of Neurocytology · doi:10.1007/bf01206897 · Cited by 216
Motor neurone sprouting induced by prolonged tetrodotoxin block of nerve action potentials
Brown, M. C., & Ironton, R. (1977) · Nature · doi:10.1038/265459a0 · Cited by 214
Sustained increase in intracellular calcium promotes neuronal survival
Collins, F., Schmidt, M., Guthrie, P., & Kater, S. B. (1991) · Journal of Neuroscience · doi:10.1523/jneurosci.11-08-02582.1991 · Cited by 206
Regulation of neuronal growth cone filopodia by intracellular calcium
Rehder, V., & Kater, S. B. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-08-03175.1992 · Cited by 177
Mattson, M., Taylor-Hunter, A., & Kater, S. B. (1988) · Journal of Neuroscience · doi:10.1523/jneurosci.08-05-01704.1988 · Cited by 164
Increased Neuromuscular Activity Reduces Sprouting in Partially Denervated Muscles
Tam, S. L., Archibald, V., Jassar, B. S., Tyreman, N., & Gordon, T. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-02-00654.2001 · Cited by 148
Self-citationHalstead, L. S. (1998) · Scientific American · doi:10.1038/scientificamerican0498-42 · Cited by 147
Synapse–Glia Interactions at the Mammalian Neuromuscular Junction
Rochon, D., Rousse, I., & Robitaille, R. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-11-03819.2001 · Cited by 145
Mechanisms controlling axonal sprouting at the neuromuscular junction
Tam, S. L., & Gordon, T. (2003) · Journal of Neurocytology · doi:10.1023/b:neur.0000020635.41233.0f · Cited by 131
Self-citationA central role for denervated tissues in causing nerve sprouting
Brown, M. C., & Holland, R. L. (1979) · Nature · doi:10.1038/282724a0 · Cited by 130
Motor unit numbers and contractile properties after spinal cord injury
Yang, J. F., Stein, R. B., Jhamandas, J. H., et al. (1990) · Annals of Neurology · doi:10.1002/ana.410280405 · Cited by 127
Research and clinical aspects of the late effects of poliomyelitis
Halstead, L. S., & Wiechers, D. O. (1986) · OSTI OAI (U.S. Department of Energy Office of Scientific and Technical Information) · Cited by 118
Love, F. M., Son, Y., & Thompson, W. J. (2003) · Journal of Neurobiology · doi:10.1002/neu.10191 · Cited by 112
Proportional enlargement of motor units after partial denervation of cat triceps surae muscles
Rafuse, V. F., Gordon, T., & Orozco, R. (1992) · Journal of Neurophysiology · doi:10.1152/jn.1992.68.4.1261 · Cited by 112
Self-citationPostsynaptic Transmission Block Can Cause Terminal Sprouting of a Motor Nerve
Holland, R. L., & Brown, M. C. (1980) · Science · doi:10.1126/science.6243417 · Cited by 93
Plasticity of Muscle Fiber and Motor Unit Types
Gordon, T., & PATTULLO, M. C. (1993) · Exercise and Sport Sciences Reviews · doi:10.1249/00003677-199301000-00011 · Cited by 86
Self-citationGlial Cells Promote Muscle Reinnervation by Responding to Activity-Dependent Postsynaptic Signals
Love, F. M., & Thompson, W. J. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-23-10390.1999 · Cited by 82
Rodnight, R., Gonçalves, C. A., Wofchuk, S. T., & Leal, R. B. (1997) · Brazilian Journal of Medical and Biological Research · doi:10.1590/s0100-879x1997000300005 · Cited by 77
Terminal sprouting of motoneurones is a local response to a local stimulus
Slack, J. R., & Pockett, S. (1981) · Brain Research · doi:10.1016/0006-8993(81)90013-5 · Cited by 60
Degenerating nerve products affect innervated muscle fibres
Brown, M. C., Holland, R. L., & Ironton, R. (1978) · Nature · doi:10.1038/275652a0 · Cited by 59
Muscarinic Control of Cytoskeleton in Perisynaptic Glia
Georgiou, J., Robitaille, R., & Charlton, M. P. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-10-03836.1999 · Cited by 57
Source of the stimulus for nerve terminal sprouting in partially denervated muscle
Pockett, S., & Slack, J. R. (1982) · Neuroscience · doi:10.1016/0306-4522(82)90239-1 · Cited by 54
Ribchester, R. R. (1988) · The Journal of Physiology · doi:10.1113/jphysiol.1988.sp017151 · Cited by 52
EFFECT OF INCREASED MOTOR ACTIVITY ON REGENERATION OF THE PERIPHERAL NERVE IN YOUNG RATS.
GUTMANN, E., & Jakoubek, B. (1963) · PubMed · Cited by 52
Calcium‐Induced Neuronal Degeneration: A Normal Growth Cone Regulating Signal Gone Awry (?)
Kater, S. B., Mattson, M., & Guthrie, P. B. (1989) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1989.tb12514.x · Cited by 44
Activity and motor unit size in partially denervated rat medial gastrocnemius
Einsiedel, L. J., & Luff, A. R. (1994) · Journal of Applied Physiology · doi:10.1152/jappl.1994.76.6.2663 · Cited by 38
Effect of exercise on stability of chronically enlarged motor units
Tam, S. L., Archibald, V., Tyreman, N., et al. (2002) · Muscle & Nerve · doi:10.1002/mus.10057 · Cited by 36
Self-citationGardiner, P. F., Michel, R. N., & Iadeluca, G. (1984) · Neuroscience Letters · doi:10.1016/0304-3940(84)90086-7 · Cited by 35
Mehta, A., Reynolds, M. L., & Woolf, C. J. (1993) · Neuroscience · doi:10.1016/0306-4522(93)90075-q · Cited by 35
Cangiano, A., Magherini, P. C., Pasino, E., et al. (1984) · The Journal of Physiology · doi:10.1113/jphysiol.1984.sp015423 · Cited by 35
Ca2+ dynamics in neuronal growth cones: Regulation and changing patterns of Ca2+ entry
Connor, J. A., Kater, S. B., Cohan, C. S., et al. (1990) · Cell Calcium · doi:10.1016/0143-4160(90)90074-5 · Cited by 30
The effect of muscle activity on motor unit size in partially denervated rat soleus muscles
Connold, A. L., & Vrbová, G. (1990) · Neuroscience · doi:10.1016/0306-4522(90)90161-v · Cited by 23
Soucy, M., Seburn, K. L., & Gardiner, P. F. (1996) · Canadian Journal of Applied Physiology · doi:10.1139/h96-018 · Cited by 22
Connold, A. L., & Vrbovà, G. (1991) · The Journal of Physiology · doi:10.1113/jphysiol.1991.sp018461 · Cited by 21
Flagged first, then by citations
Research works printed but not linked: 2
- Rabben I, 1997, Distribution of extrajunctional acetylcholine receptors in rat skeletal muscle after inactivation by botulinum toxin, Soc Neurosci Abstr, 23, 154
- Tam SL, 1998, Detrimental effect of neuromuscular activity on the ability of terminal Schwann cells to induce sprouting in extensively denervated tibialis anterior muscle, Soc Neurosci Abstr, 24, 413.16
Cited by
Sorted by citations
Aagaard, P., Suetta, C., Caserotti, P., Magnusson, S. P., & Kjær, M. (2010) · Scandinavian Journal of Medicine & Science in Sports · doi:10.1111/j.1600-0838.2009.01084.x · Cited by 709
Safety of long-term electrical peripheral nerve stimulation: review of the state of the art
Günter, C., Delbeke, J., & Ortiz-Catalan, M. (2019) · Journal of NeuroEngineering and Rehabilitation · doi:10.1186/s12984-018-0474-8 · Cited by 198
Neuroprotective Effects of Exercise Treatments after Injury: The Dual Role of Neurotrophic Factors
Cobianchi, S., Arbat-Plana, A., Lopez-Alvarez, V. M., & Navarro, X. (2017) · Current Neuropharmacology · doi:10.2174/1570159x14666160330105132 · Cited by 94
Metadata
- Authors
- Tam, S. L., & Gordon, T.
- Affiliations
- University of Alberta (CA)
- Corresponding author
- Gordon, T.
- ORCID
- Gordon, T.
- Venue
- Journal of Neurobiology
- Publisher
- Wiley
- Published
- 2003-10-06
- Volume
- 57
- Issue
- 2
- Pages
- 221-234
- ISSN
- 0022-3034 (ISSN-L)
- 1097-4695
- OpenAlex
- W2076384214
- Cited by
- 70
- References
- 47
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 3 · 2023: 1 · 2022: 3 · 2021: 1 · 2020: 4 · 2019: 4 · 2018: 3 · 2017: 3 · 2016: 10 · 2015: 5 · 2014: 5 · 2013: 2 · 2012: 1
- FWCI
- 0.46
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Neurobiology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Nerve injury and regeneration
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Health Sciences › Medicine › Genetics (clinical) › Neurogenetic and Muscular Disorders Research
- Keywords
- axonal sprouting, partial denervation, neuromuscular activity, Schwann cells, perisynaptic Schwann cells, tibialis anterior, running, reinnervation
- MeSH terms
- Animals, Female, Hindlimb, Immunohistochemistry, Motor Activity, Motor Endplate, Muscle Denervation, Nerve Regeneration, Schwann Cells, Time Factors, Rats, Sprague-Dawley, Muscle, Skeletal, 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