Motor skill learning requires active central myelination
Open accessAbstract
Myelin-forming oligodendrocytes (OLs) are formed continuously in the healthy adult brain. In this work, we study the function of these late-forming cells and the myelin they produce. Learning a new motor skill (such as juggling) alters the structure of the brain’s white matter, which contains many OLs, suggesting that late-born OLs might contribute to motor learning. Consistent with this idea, we show that production of newly formed OLs is briefly accelerated in mice that learn a new skill (running on a “complex wheel” with irregularly spaced rungs). By genetically manipulating the transcription factor myelin regulatory factor in OL precursors, we blocked production of new OLs during adulthood without affecting preexisting OLs or myelin. This prevented the mice from mastering the complex wheel. Thus, generation of new OLs and myelin is important for learning motor skills.
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In the mouse, motor learning or motor behavioral improvements require proliferation and differentiation of oligodendrocyte precursor cells in the white matter and motor cortex.
“In the mouse, motor learning or motor behavioral improvements require proliferation and differentiation of oligodendrocyte precursor cells (OPCs) in the white matter and motor cortex (Gibson et al., 2014 ; McKenzie et al., 2014 ; Xiao et al., 2016 ).”
From Motor learning requires myelination to reduce asynchrony and spontaneity in neural activity (2020) · cites this paper as McKenzie et al., 2014
In “Running stimulates OP proliferation and OL production” (page unavailable), complex-wheel running increased precursor proliferation and oligodendrocyte production in the corpus callosum. The Abstract reports that blocking new oligodendrocyte production prevented mice from mastering the wheel, and “Preventing adult myelination by conditional deletion of myelin regulatory factor” also documents reduced production in motor cortex. The paper does not establish that precursor proliferation itself is required, or that the motor-cortex change specifically causes the learning deficit. (LLM, conf=0.85)
Experimental — accuracy not yet measuredThe proliferation and differentiation of M1 OPCs is accelerated during motor learning.
“We focused on the primary motor cortex (M1), as the proliferation and differentiation of M1 OPCs is accelerated, and the activity of M1 cortical neurons dynamically changes during motor learning (Huber et al., 2012 ; Masamizu et al., 2014 ; McKenzie et al., 2014 ; Peters, Chen, & Komiyama, 2014 ; Xiao et al., 2016 ).”
From Motor learning requires myelination to reduce asynchrony and spontaneity in neural activity (2020) · cites this paper as McKenzie et al., 2014
In “Running stimulates OP proliferation and OL production” (page not available), the paper reports increased precursor proliferation and newly formed oligodendrocytes during wheel running, but those measurements were made in the corpus callosum, not M1. The paper also measures oligodendrocyte production in motor cortex after genetic manipulation; that does not establish accelerated M1 OPC proliferation and differentiation during learning. (LLM, conf=0.89)
Experimental — accuracy not yet measuredIn such a case, the synchronous input of myelinated long-range axons connecting distant areas, and information processes with a high signal-to-noise ratio, may be important.
“In such a case, the synchronous input of myelinated long‐range axons connecting distant areas, and information processes with a high signal‐to‐noise ratio, may be important (Gibson et al., 2014 ; McKenzie et al., 2014 ; Xiao et al., 2016 ).”
From Motor learning requires myelination to reduce asynchrony and spontaneity in neural activity (2020) · cites this paper as McKenzie et al., 2014
The paper’s introductory text says myelin speeds electrical communication, and the section “Running stimulates OP proliferation and OL production” suggests that activity-dependent myelination could make motor circuits more efficient (page unavailable in our copy). It does not address synchronous input from long-range axons connecting distant areas or a high signal-to-noise ratio. (LLM, conf=0.85)
Experimental — accuracy not yet measuredThese studies assessed motor learning ability using a running wheel with irregularly spaced rungs, in which the mice had to coordinate many parts of the body to avoid missing their step, even in the first session.
“These assessed motor learning ability using a running wheel with irregularly spaced rungs, in which the mice had to coordinate many parts of the body to avoid missing their step, even in the first session.”
From Motor learning requires myelination to reduce asynchrony and spontaneity in neural activity (2020) · cites this paper as McKenzie et al., 2014
In “The complex running wheel” (page not provided), the paper explicitly says it assessed motor learning with irregularly spaced rungs and describes mice coordinating their forepaws and hindpaws to find a rung. It says mice had great difficulty at first, but does not establish that they used this successful coordination in the first session. (LLM, conf=0.84)
Experimental — accuracy not yet measuredIn the complex wheel paradigm, running leads to an increase in proliferating OPCs after 4 days, followed by an increase in oligodendrocytes after 8 days.
“running on the wheel leads to an increase in the number of proliferating OPCs after 4 days, followed by an increase in oligodendrocytes after 8 days (20).”
From Oligodendrocyte heterogeneity in the mouse juvenile and adult central nervous system (2016) · cites this paper as [20]
In “Running stimulates OP proliferation and OL production” (page unavailable), the paper reports an increased fraction of EdU-labeled OPCs after 4 days on the complex wheel, consistent with increased proliferation. It reports an increase in the absolute number of OPCs at 6 days and in oligodendrocyte-lineage cells at 11 days, not an increase in oligodendrocytes at 8 days. (LLM, conf=0.90)
Experimental — accuracy not yet measured
Increased motor skills were apparent after 2 days in wild type mice, but not in mutant mice unable to synthesize new myelin.
“increased motor skills were already apparent after 2 days in wild type mice, but not in mutant mice that were unable to synthesize new myelin (20)”
From Oligodendrocyte heterogeneity in the mouse juvenile and adult central nervous system (2016) · cites this paper as [20]
In “Active myelination is required for motor skill learning” (page unavailable), the paper reports that Myrf-mutant mice performed worse than their control littermates on the complex wheel. It does not establish the claimed two-day milestone, and it says both groups improved during the first week—not that the mutants showed no improvement. The controls were Myrf(+/−) littermates, rather than wild-type mice. (LLM, conf=0.88)
Experimental — accuracy not yet measuredThe density of BCAS1+ oligodendrocytes in the cortex remains high throughout life, in contrast to white matter, supporting a physiological role in neuronal function.
“the density of BCAS1+ oligodendrocytes in the cortex remains high throughout life—in stark contrast to the white matter—supporting a physiological role in neuronal function, e.g. as effectors of adaptive cortical myelination and circuit modulation.49,50”
From BCAS1-positive oligodendrocytes enable efficient cortical remyelination in multiple sclerosis (2025) · cites this paper as [50]
The Abstract and “Running stimulates OP proliferation and OL production” section support a role for newly formed oligodendrocytes and myelination in motor learning, and discuss activity-dependent myelination as a possible mechanism. Our copy does not identify BCAS1+ cells or show that their density remains high throughout life in cortex, in contrast to white matter (searched: BCAS1, cortical density, adaptive cortical myelination). No page numbers were available in our copy. (LLM, conf=0.86)
Experimental — accuracy not yet measuredTask learning can alter dMRI attributes.
“It is now known that task learning can alter dMRI attributes (Hofstetter et al., 2013; McKenzie et al., 2014; Sampaio-Baptista et al., 2013; Xiao et al., 2016)”
From The cingulum bundle: Anatomy, function, and dysfunction (2018) · cites this paper as McKenzie et al., 2014
The Abstract reports MRI-detected white-matter changes during motor training, and the discussion cites MRI evidence of changes during several kinds of learning. Our copy does not identify those measurements as diffusion MRI or specify dMRI attributes, so it supports the learning-related MRI change but not the more specific dMRI claim. (LLM, conf=0.82)
Experimental — accuracy not yet measuredOngoing myelin remodeling throughout life may be important for learning, behavior, and cognition throughout adulthood.
“Recent evidence in animal models indicates that ongoing myelin remodeling throughout life may be important for learning, behavior, and cognition throughout adulthood (Liu et al., 2012; McKenzie et al., 2014).”
From Down Syndrome Developmental Brain Transcriptome Reveals Defective Oligodendrocyte Differentiation and Myelination (2016) · cites this paper as McKenzie et al., 2014
The Abstract (page not provided) says that oligodendrocytes continue to form throughout life and that active myelination in adult mice is required for motor skill learning. The paper does not establish that myelin remodeling is important for behavior or cognition more broadly throughout adulthood; the ‘Running stimulates OP proliferation and OL production’ section says other types of learning remain to be tested. (LLM, conf=0.86)
Experimental — accuracy not yet measuredGenetic deletion of myelin regulatory factor causes deficient maturation of OPCs in mature mice, resulting in impaired motor learning.
“Genetic deletion of myelin regulatory factor causes deficient maturation of OPCs in mature mice, resulting in impaired motor learning (McKenzie et al., 2014 ; Xiao et al., 2016 ).”
From Motor learning requires myelination to reduce asynchrony and spontaneity in neural activity (2020) · cites this paper as McKenzie et al., 2014
In contrast to our results, the effect of impaired myelin regulation was detected from the beginning of motor training in other studies.
“In contrast to our results, the effect of impaired myelin regulation was detected from the beginning of motor training in other studies (McKenzie et al., 2014 ; Xiao et al., 2016 ).”
From Motor learning requires myelination to reduce asynchrony and spontaneity in neural activity (2020) · cites this paper as McKenzie et al., 2014
The complex wheel paradigm requires active myelination.
“a process that requires active myelination (20).”
From Oligodendrocyte heterogeneity in the mouse juvenile and adult central nervous system (2016) · cites this paper as [20]
Oligodendrocyte lineage cells contribute to learning already within the first 2 days.
“suggesting that oligodendrocyte lineage cells contribute to learning already within the first 2 days.”
From Oligodendrocyte heterogeneity in the mouse juvenile and adult central nervous system (2016) · cites this paper as [20]
Experience can alter white matter microstructure.
“Indeed, the growing realisation that experience can alter white matter microstructure (Metzler-Baddeley et al., 2017; (McKenzie et al., 2014) Zatorre et al., 2012) highlights the problems of separating cause from effect.”
From The cingulum bundle: Anatomy, function, and dysfunction (2018) · cites this paper as McKenzie et al., 2014
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- Authors
- McKenzie, I. A., Ohayon, D., Li, H., Paes de Faria, J., Emery, B., Tohyama, K., & Richardson, W. D.
- Affiliations
- University College London (GB)
- The Wolfson Institute for Biomedical Research, University College London, Gower Street, London WC1E 6BT, UK.
- The University of Melbourne (AU)
- Iwate Medical University (JP)
- Corresponding author
- McKenzie, Ian A.
- Ohayon, David
- Richardson, William D.
- Venue
- Science
- Published
- 2014-10-17
- Volume
- 346
- Issue
- 6207
- Pages
- 318-322
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- PMC
- PMC6324726
- OpenAlex
- W2085529478
- Cited by
- 1,177
- References
- 36
- Citations by year
- 2026: 68 · 2025: 90 · 2024: 103 · 2023: 107 · 2022: 101 · 2021: 146 · 2020: 108 · 2019: 122 · 2018: 83 · 2017: 101 · 2016: 88 · 2015: 53 · 2014: 3 · 2012: 1
- FWCI
- 28.41
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- HAL (submittedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Funders
- Wellcome Trust (100269, 100269/Z/12/Z, 066745)
- Biotechnology and Biological Sciences Research Council (BB/L003236/1)
- Japan Society for the Promotion of Science (24650181)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
- Health Sciences › Medicine › Pathology and Forensic Medicine › Multiple Sclerosis Research Studies
- Keywords
- motor skill learning, oligodendrocyte myelination, adult neurogenesis, white matter plasticity, oligodendrocyte precursor cells, juggling
- MeSH terms
- Animals, Brain, Humans, Learning, Male, Mice, Transgenic, Motor Skills, Myelin Sheath, Synaptic Transmission, Oligodendroglia, Mental Recall, Transcription Factors, Gene Deletion, Cell Proliferation, Mice
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