Induction of myelination in the central nervous system by electrical activity
Open accessAbstract
The oligodendrocyte is the myelin-forming cell in the central nervous system. Despite the close interaction between axons and oligodendrocytes, there is little evidence that neurons influence myelinogenesis. On the contrary, newly differentiated oligodendrocytes, which mature in culture in the total absence of neurons, synthesize the myelin-specific constituents of oligodendrocytes differentiated in vivo and even form myelin-like figures. Neuronal electrical activity may be required, however, for the appropriate formation of the myelin sheath. To investigate the role of electrical activity on myelin formation, we have used highly specific neurotoxins, which can either block (tetrodotoxin) or increase (alpha-scorpion toxin) the firing of neurons. We show that myelination can be inhibited by blocking the action potential of neighboring axons or enhanced by increasing their electrical activity, clearly linking neuronal electrical activity to myelinogenesis.
Integrity signals
Registry
Cites
Statistics
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?
Changes in the cellular organization of a brain region can result from molecular processes that follow neuronal activity.
“Although changes in the cellular organization of a specific brain region can result from the molecular processes after neuronal activity (65,68)”
From Neuroanatomic differences associated with stress susceptibility and resilience (2016) · cites this paper as [68]
Cites
Growth of a rat neuroblastoma cell line in serum-free supplemented medium.
Bottenstein, J. E., & SATO, G. H. (1979) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.76.1.514 · Cited by 2,282 · see citing works
Wiesel, T. N., & Hubel, D. H. (1965) · Journal of Neurophysiology · doi:10.1152/jn.1965.28.6.1029 · Cited by 1,598 · see citing works
Neurotoxins that Act on Voltage-Sensitive Sodium Channels in Excitable Membranes
Catterall, W. A. (1980) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev.pa.20.040180.000311 · Cited by 1,248 · see citing works
The oligodendrocyte and its many cellular processes
Pfeiffer, S. E., Warrington, A. E., & Bansal, R. (1993) · Trends in Cell Biology · doi:10.1016/0962-8924(93)90213-k · Cited by 852 · see citing works
Impulse activity and the patterning of connections during cns development
Shatz, C. J. (1990) · Neuron · doi:10.1016/0896-6273(90)90333-b · Cited by 766 · see citing works
Proliferation of oligodendrocyte precursor cells depends on electrical activity in axons
Barres, B. A., & Raff, M. C. (1993) · Nature · doi:10.1038/361258a0 · Cited by 673 · see citing works
Multiple sclerosis: Remyelination of nascent lesions: Remyelination of nascent lesions
Prineas, J. W., Barnard, R. O., Kwon, E. E., Sharer, L. R., & Cho, E. ‐. (1993) · Annals of Neurology · doi:10.1002/ana.410330203 · Cited by 574 · see citing works
Dong, Z., Brennan, A., Liu, N., Yarden, Y., Lefkowitz, G. K., Mirsky, R., & Jessen, K. R. (1995) · Neuron · doi:10.1016/0896-6273(95)90147-7 · Cited by 445 · see citing works
Myelin-specific proteins and glycolipids in rat Schwann cells and oligodendrocytes in culture.
Mirsky, R., Winter, J., Abney, E. R., Pruss, R. M., Gavrilović, J., & RAFF, M. C. (1980) · The Journal of Cell Biology · doi:10.1083/jcb.84.3.483 · Cited by 441 · see citing works
Patterns of oligodendroglia pathology in multiple sclerosis
Ozawa, K., Suchanek, G., Breitschopf, H., Br€ck, W., Budka, H., Jellinger, K. A., & Lassmann, H. (1994) · Brain · doi:10.1093/brain/117.6.1311 · Cited by 404 · see citing works
Ion Channels in Vertebrate Glia
Barres, B. A., Chun, L. L. Y., & Corey, D. P. (1990) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.13.030190.002301 · Cited by 355 · see citing works
Emergence of three myelin proteins in oligodendrocytes cultured without neurons.
Dubois-Dalcq, M. E., Behar, T. N., Hudson, L. D., & Lazzarini, R. A. (1986) · The Journal of Cell Biology · doi:10.1083/jcb.102.2.384 · Cited by 342 · see citing works
Matteoli, M., Takei, K., Perin, M., Südhof, T., & Camilli, P. D. (1992) · Journal of Cell Biology · doi:10.1083/jcb.117.4.849 · Cited by 326 · see citing works
A novel myelin-associated glycoprotein defined by a mouse monoclonal antibody
Linington, C., Webb, M. H., & Woodhams, P. L. (1984) · Journal of Neuroimmunology · doi:10.1016/0165-5728(84)90064-x · Cited by 323 · see citing works
Does oligodendrocyte survival depend on axons?
Barres, B. A., Jacobson, M. D., Schmid, R., Sendtner, M., & RAFF, M. C. (1993) · Current Biology · doi:10.1016/0960-9822(93)90039-q · Cited by 299 · see citing works
Multiple sclerosis. Oligodendrocyte survival and proliferation in an active established lesion.
Raine, C. S., Scheinberg, L. C., & Waltz, J. M. (1981) · PubMed · Cited by 264 · see citing works
Aguayo, A. J., Charron, L., & Bray, G. M. (1976) · Journal of Neurocytology · doi:10.1007/bf01175570 · Cited by 259 · see citing works
Reynolds, R., & Wilkin, G. P. (1988) · Development · doi:10.1242/dev.102.2.409 · Cited by 256 · see citing works
Schwann cell precursors and their development
Jessen, K. R., & Mirsky, R. (1991) · Glia · doi:10.1002/glia.440040210 · Cited by 256 · see citing works
Differential Localization of MAP‐2 and Tau in Mammalian Neurons in Situ a
Binder, L. I., Frankfurter, A. J., & Rebhun, L. I. (1986) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1986.tb38392.x · Cited by 210 · see citing works
Kiss, J. Z., Wang, C., Olive, S., Rougon, G. N., Lang, J., Baetens, D., Harry, D., & Pralong, W. F. (1994) · The EMBO Journal · doi:10.1002/j.1460-2075.1994.tb06862.x · Cited by 153 · see citing works
GYLLENSTEN, L. J., & Malmfors, T. (1963) · Development · doi:10.1242/dev.11.1.255 · Cited by 148 · see citing works
Axons regulate Schwann cell expression of the POU transcription factor SCIP
Scherer, S., Wang, D., Kuhn, R., et al. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-04-01930.1994 · Cited by 136 · see citing works
Even in culture, oligodendrocytes myelinate solely axons.
Lubetzki, C., Demerens, C., Anglade, P., Villarroya, H., Frankfurter, A. J., Lee, V. M., & Zalc, B. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.14.6820 · Cited by 129 · see citing works
Self-citationEvidence that axons are mitogenic for oligodendrocytes isolated from adult animals
Wood, P. M., & Bunge, R. P. (1986) · Nature · doi:10.1038/320756a0 · Cited by 114 · see citing works
Myelination in rabbit optic nerves is accelerated by artificial eye opening
Tauber, H., Waehneldt, T. V., & NEUHOFF, V. (1980) · Neuroscience Letters · doi:10.1016/0304-3940(80)90003-8 · Cited by 102 · see citing works
Evidence for an early role for myelin‐associated glycoprotein in the process of myelination
Owens, G. C., & Bunge, R. P. (1989) · Glia · doi:10.1002/glia.440020208 · Cited by 101 · see citing works
Wood, P. M., & Williams, A. K. (1984) · Developmental Brain Research · doi:10.1016/0165-3806(84)90045-2 · Cited by 88 · see citing works
Monge, M., Kadiiski, D., Jacque, C., et al. (1987) · Developmental Neuroscience · doi:10.1159/000112255 · Cited by 87 · see citing works
Colello, R. J., Devey, L. R., Imperato, E. L., & Pott, U. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-11-07665.1995 · Cited by 85 · see citing works
Expression of myelin proteolipid and basic protein mRNAS in cultured cells
Macklin, W. B., Weill, C. L., & Deininger, P. L. (1986) · Journal of Neuroscience Research · doi:10.1002/jnr.490160118 · Cited by 83 · see citing works
Dargent, B., & Couraud, F. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.15.5907 · Cited by 80 · see citing works
Self-citationSarliève, L. L., Rao, G. S., Campbell, G. L., et al. (1980) · Brain Research · doi:10.1016/0006-8993(80)90008-6 · Cited by 70 · see citing works
Szuchet, S., Polak, P. E., & Yim, S. H. (1987) · Developmental Neuroscience · doi:10.1159/000112254 · Cited by 66 · see citing works
Berwald‐Netter, Y., Martin‐Moutôt, N., Koulakoff, A., et al. (1981) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.78.2.1245 · Cited by 60 · see citing works
Isolation and cultivation of mature oligodendroglial cells
Althaus, H. H., Montz, H. P. M., NEUHOFF, V., & Schwartz, P. J. (1984) · Die Naturwissenschaften · doi:10.1007/bf00396614 · Cited by 46 · see citing works
Axons modulate the expression of proteolipid protein in the CNS
Scherer, S. S., Vogelbacker, H. H., & Kamholz, J. A. (1992) · Journal of Neuroscience Research · doi:10.1002/jnr.490320203 · Cited by 44 · see citing works
Functional evidence for the role of axolemma in CNS myelination
Notterpek, L. M., & Rome, L. H. (1994) · Neuron · doi:10.1016/0896-6273(94)90361-1 · Cited by 41 · see citing works
Lubetzki, C., Goujet‐Zalc, C., Demerens, C., Danos, O., & Zalc, B. (1992) · Glia · doi:10.1002/glia.440060407 · Cited by 30 · see citing works
Self-citationScherer, M., Heller, M., & Schachner, M. (1992) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1992.tb00905.x · Cited by 20 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Biology of Oligodendrocyte and Myelin in the Mammalian Central Nervous System
Baumann, N., & Pham-Dinh, D. (2001) · Physiological Reviews · doi:10.1152/physrev.2001.81.2.871 · Cited by 1,828 · see citing works
Training induces changes in white-matter architecture
Scholz, J., Klein, M. C., Behrens, T. E. J., & Johansen-Berg, H. (2009) · Nature Neuroscience · doi:10.1038/nn.2412 · Cited by 1,508 · see citing works
Neuronal activity promotes oligodendrogenesis and adaptive myelination in the mammalian brain
Gibson, E. M., Purger, D., Mount, C. W., Goldstein, A. K., Lin, G. L., Wood, L. S., Inema, I., Miller, S. E., Bieri, G., Zuchero, J. B., et al. (2014) · Science · doi:10.1126/science.1252304 · Cited by 1,472 · see citing works
White matter in learning, cognition, and psychiatric disorders
Fields, R. D. (2008) · Trends in Neurosciences · doi:10.1016/j.tins.2008.04.001 · Cited by 1,337 · see citing works
Extensive piano practicing has regionally specific effects on white matter development
Bengtsson, S. L., Nagy, Z., Skare, S., Forsman, L., Forssberg, H., & Ullén, F. (2005) · Nature Neuroscience · doi:10.1038/nn1516 · Cited by 1,193 · see citing works
Longitudinal Development of Human Brain Wiring Continues from Childhood into Adulthood
Lebel, C., & Beaulieu, C. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.5302-10.2011 · Cited by 1,193 · see citing works
Oligodendrocytes: biology and pathology
Bradl, M., & Lassmann, H. (2010) · Acta Neuropathologica · doi:10.1007/s00401-009-0601-5 · Cited by 933 · see citing works
Dubois, J., Dehaene-Lambertz, G., Kulikova, S., Poupon, C., Hüppi, P. S., & Hertz-Pannier, L. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2013.12.044 · Cited by 851 · see citing works
Regulation of oligodendrocyte differentiation and myelination
Emery, B. (2010) · Science · doi:10.1126/science.1190927 · Cited by 653 · see citing works
Control of local protein synthesis and initial events in myelination by action potentials
Wake, H., Lee, P. R., & Fields, R. D. (2011) · Science · doi:10.1126/science.1206998 · Cited by 636 · see citing works
Blalock, E. M., Chen, K.-C., Sharrow, K., Herman, J. P., Porter, N. M., Foster, T. C., & Landfield, P. W. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-09-03807.2003 · Cited by 570 · see citing works
Dynamics of Oligodendrocyte Generation and Myelination in the Human Brain
Yeung, M. S. Y., Zdunek, S., Bergmann, O., Bernard, S., Salehpour, M., Alkass, K., Perl, S., Tisdale, J., Possnert, G., Brundin, L., et al. (2014) · Cell · doi:10.1016/j.cell.2014.10.011 · Cited by 541 · see citing works
Training of Working Memory Impacts Structural Connectivity
Takeuchi, H., Sekiguchi, A., Taki, Y., Yokoyama, S., Yomogida, Y., Komuro, N., Yamanouchi, T., Suzuki, S., & Kawashima, R. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.4611-09.2010 · Cited by 531 · see citing works
Oligodendrocyte-Encoded HIF Function Couples Postnatal Myelination and White Matter Angiogenesis
Yuen, T. J., Silbereis, J. C., Griveau, A., Chang, S. M., Daneman, R., Fancy, S. P. J., Zahed, H., Maltepe, E., & Rowitch, D. H. (2014) · Cell · doi:10.1016/j.cell.2014.04.052 · Cited by 433 · see citing works
Disruption of oligodendrogenesis impairs memory consolidation in adult mice
Steadman, P. E., Xia, F., Ahmed, M., Mocle, A. J., Penning, A. R. A., Geraghty, A. C., Steenland, H. W., Monje, M., Josselyn, S. A., & Frankland, P. W. (2020) · Neuron · doi:10.1016/j.neuron.2019.10.013 · Cited by 426 · see citing works
van der Knaap, M. S., & Bugiani, M. (2017) · Acta Neuropathologica · doi:10.1007/s00401-017-1739-1 · Cited by 403 · see citing works
Olesen, P. J., Nagy, Z., Westerberg, H., & Klingberg, T. (2003) · Cognitive Brain Research · doi:10.1016/j.cogbrainres.2003.09.003 · Cited by 397 · see citing works
Synaptic vesicle release regulates myelin sheath number of individual oligodendrocytes in vivo
Mensch, S., Baraban, M., Almeida, R., Czopka, T., Ausborn, J., El Manira, A., & Lyons, D. A. (2015) · Nature Neuroscience · doi:10.1038/nn.3991 · Cited by 398 · see citing works
Role of myelin plasticity in oscillations and synchrony of neuronal activity
Pajevic, S., Basser, P. J., & Fields, R. D. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2013.11.007 · Cited by 378 · see citing works
Oligodendrocyte development and the onset of myelination in the human fetal brain
Jakovcevski, I. (2009) · Frontiers in Neuroanatomy · doi:10.3389/neuro.05.005.2009 · Cited by 323 · see citing works
Myelin plasticity and nervous system function
Monje, M. (2018) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-080317-061853 · Cited by 274 · see citing works
Charles, P., Hernandez, M. P., Stankoff, B., Aigrot, M. S., Colin, C., Rougon, G., Zalc, B., & Lubetzki, C. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.100076197 · Cited by 306 · see citing works
Self-citationTranscriptional Convergence of Oligodendrocyte Lineage Progenitors during Development
Marques, S., van Bruggen, D., Vanichkina, D. P., Floriddia, E. M., Munguba, H., Väremo, L., Giacomello, S., Falcão, A. M., Meijer, M., Björklund, Å. K., et al. (2018) · Developmental Cell · doi:10.1016/j.devcel.2018.07.005 · Cited by 290 · see citing works
Engvig, A., Fjell, A. M., Westlye, L. T., Moberget, T., Sundseth, Ø., Larsen, V. A., & Walhovd, K. B. (2012) · Human Brain Mapping · doi:10.1002/hbm.21370 · Cited by 250 · see citing works
Fard, M. K., van der Meer, F., Sánchez, P., Cantuti-Castelvetri, L., Mandad, S., Jäkel, S., Fornasiero, E. F., Schmitt, S., Ehrlich, M., Starost, L., et al. (2017) · Science Translational Medicine · doi:10.1126/scitranslmed.aam7816 · Cited by 247 · see citing works
Experience-dependent plasticity of white-matter microstructure extends into old age
Lövdén, M., Bodammer, N. C., Kühn, S., Kaufmann, J., Schütze, H., Tempelmann, C., Heinze, H.-J., Düzel, E., Schmiedek, F., & Lindenberger, U. (2010) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2010.08.026 · Cited by 222 · see citing works
On Myelinated Axon Plasticity and Neuronal Circuit Formation and Function
Almeida, R. G., & Lyons, D. A. (2017) · The Journal of Neuroscience · doi:10.1523/jneurosci.3185-16.2017 · Cited by 221 · see citing works
Neuronal effects following working memory training.
Buschkuehl, M., Jaeggi, S. M., & Jonides, J. (2012) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2011.10.001 · Cited by 212 · see citing works
Enhanced brain connectivity in long-term meditation practitioners
Luders, E., Clark, K., Narr, K. L., & Toga, A. W. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2011.05.075 · Cited by 209 · see citing works
Krogsrud, S. K., Fjell, A. M., Tamnes, C. K., Grydeland, H., Mork, L., Due-Tønnessen, P., Bjørnerud, A., Sampaio-Baptista, C., Andersson, J., Johansen-Berg, H., et al. (2016) · NeuroImage · doi:10.1016/j.neuroimage.2015.09.017 · Cited by 190 · see citing works
Neuroanatomic differences associated with stress susceptibility and resilience
Anacker, C., Scholz, J., O’Donnell, K. J., Allemang-Grand, R., Diorio, J., Bagot, R. C., Nestler, E. J., Hen, R., Lerch, J. P., & Meaney, M. J. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.08.009 · Cited by 167 · see citing works
White matter development and early cognition in babies and toddlers
O'Muircheartaigh, J., Dean, D. C., Ginestet, C. E., Walker, L., Waskiewicz, N., Lehman, K., Dirks, H., Piryatinsky, I., & Deoni, S. C. L. (2014) · Human Brain Mapping · doi:10.1002/hbm.22488 · Cited by 183 · see citing works
Clarke, L. E., Young, K. M., Hamilton, N. B., Li, H., Richardson, W. D., & Attwell, D. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.0928-12.2012 · Cited by 182 · see citing works
Relating imaging indices of white matter integrity and volume in healthy older adults
Hugenschmidt, C. E., Peiffer, A. M., Kraft, R. A., Casanova, R., Deibler, A. R., Burdette, J. H., Maldjian, J. A., & Laurienti, P. J. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhm080 · Cited by 166 · see citing works
Figlia, G., Gerber, D., & Suter, U. (2018) · Glia · doi:10.1002/glia.23273 · Cited by 165 · see citing works
Exploring the Early Organization and Maturation of Linguistic Pathways in the Human Infant Brain
Dubois, J., Poupon, C., Thirion, B., Simonnet, H., Kulikova, S., Leroy, F., Hertz-Pannier, L., & Dehaene-Lambertz, G. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhv082 · Cited by 165 · see citing works
Walhovd, K. B., Johansen-Berg, H., & Káradóttir, R. T. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.06.058 · Cited by 156 · see citing works
Li, Q., Brus-Ramer, M., Martin, J. H., & McDonald, J. W. (2010) · Neuroscience Letters · doi:10.1016/j.neulet.2010.05.043 · Cited by 150 · see citing works
Noori, R., Park, D., Griffiths, J. D., Bells, S., Frankland, P. W., Mabbott, D., & Lefebvre, J. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1916646117 · Cited by 137 · see citing works
Vincze, A., Mázló, M., Seress, L., Komoly, S., & Ábrahám, H. (2008) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2008.05.003 · Cited by 85 · see citing works
Stys, P. K. (2011) · Trends in Neurosciences · doi:10.1016/j.tins.2011.06.004 · Cited by 51 · see citing works
From bed to bench side: Reverse translation to optimize neuromodulation for mood disorders
Rudebeck, P. H., Rich, E. L., & Mayberg, H. S. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1902287116 · Cited by 42 · see citing works
- Authors
- Demerens, C., Stankoff, B., Logak, M., Anglade, P., Allinquant, B., Couraud, F., Zalc, B., & Lubetzki, C.
- Affiliations
- Inserm (FR)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 1996-09-03
- Volume
- 93
- Issue
- 18
- Pages
- 9887-9892
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC38524
- OpenAlex
- W2023693164
- Cited by
- 678
- References
- 40
- Citations by year
- 2026: 13 · 2025: 17 · 2024: 21 · 2023: 15 · 2022: 24 · 2021: 38 · 2020: 40 · 2019: 36 · 2018: 38 · 2017: 55 · 2016: 35 · 2015: 35 · 2014: 37 · 2013: 30 · 2012: 22
- FWCI
- 2.34
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Health Sciences › Medicine › Pathology and Forensic Medicine › Multiple Sclerosis Research Studies
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- myelination, oligodendrocytes, neuronal electrical activity, action potential, tetrodotoxin, alpha-scorpion toxin, neurotoxins, central nervous system
- MeSH terms
- Action Potentials, Animals, Cells, Cultured, Central Nervous System, Electric Stimulation, Microscopy, Electron, Myelin Sheath, Optic Nerve, Potassium, Scorpion Venoms, Tetrodotoxin, Time Factors, Sodium Channels, Mice
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