Learning-related contraction of grey matter in rodent sensorimotor cortex is associated with adaptive myelination
- Umeå University, Sweden
- Karolinska Institute, Sweden
- University of Gothenburg, Sweden
Abstract
From observations in rodents, it has been suggested that the cellular basis of learning-dependent changes, detected using structural magnetic resonance imaging (MRI), may be increased dendritic spine density, alterations in astrocyte volume, and adaptations within intracortical myelin. Myelin plasticity is crucial for neurological function and active myelination is required for learning and memory. However, the dynamics of myelin plasticity and how it relates to morphometric-based measurements of structural plasticity remains unknown. We used a motor skill learning paradigm in male mice to evaluate experience-dependent brain plasticity by voxel-based morphometry (VBM) in longitudinal MRI, combined with a cross-sectional immunohistochemical investigation. Whole brain VBM revealed non-linear decreases in grey matter volume (GMV) juxtaposed to non-linear increases in white matter volume (WMV) within GM that were best modelled by an asymptotic time course. Using an atlas-based cortical mask, we found non-linear changes with learning in primary and secondary motor areas and in somatosensory cortex. Analysis of cross-sectional myelin immunoreactivity in forelimb somatosensory cortex confirmed an increase in myelin immunoreactivity followed by a return towards baseline levels. Further investigations using quantitative confocal microscopy confirmed these changes specifically to the length density of myelinated axons. The absence of significant histological changes in cortical thickness suggests that non-linear morphometric changes are likely due to changes in intracortical myelin for which morphometric WMV in somatosensory cortex significantly correlated with myelin immunoreactivity. Together, these observations indicate a non-linear increase of intracortical myelin during learning and support the hypothesis that myelin is a component of structural changes observed by VBM during learning.
Data availability
The structural MRI raw data and the scripts employed for the image processing and analysis have been uploaded to Dryad. All these files are provided together with an explanatory document that would allow to reproduce our results.
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Skilled Reaching Structural MRIDryad, doi:10.5061/dryad.crjdfn36c.
Article and author information
Author details
Daniel J Marcellino
Funding
StratNeuro
- Daniel J Marcellino
Kempestiftelserna (JCK-1922.2)
- Fahad R Sultan
- Daniel J Marcellino
Insamlingsstiftelsen för medicinsk forskning Umeå Universitet
- Daniel J Marcellino
Magnus Bergvalls Stiftelse (2016-01639)
- Daniel J Marcellino
Vetenskapsrådet (2015-01717)
- Claudio Brozzoli
Agence Nationale de la Recherche (ANR-16-CE28-0008-01)
- Claudio Brozzoli
Agencia Canaria de Investigación, Innovación y Sociedad de la Información
- Héctor Martín Estévez-Silva
Umeå University Medical Faculty
- Daniel J Marcellino
Vetenskapsrådet (2018-01047)
- Martin Lövdén
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Animal experimentation: All procedures involving animals were in accordance with protocols approved by the Umeå Regional Ethics Committee for Animal Research (ethical permit: Dnr A 35/2016).
Copyright
© 2022, Mediavilla et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Learning-related contraction of grey matter in rodent sensorimotor cortex is associated with adaptive myelination
eLife 11:e77432.
https://doi.org/10.7554/eLife.77432
Further reading
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- Neuroscience
When navigating environments with changing rules, human brain circuits flexibly adapt how and where we retain information to help us achieve our immediate goals.
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- Neuroscience
When holding visual information temporarily in working memory (WM), the neural representation of the memorandum is distributed across various cortical regions, including visual and frontal cortices. However, the role of stimulus representation in visual and frontal cortices during WM has been controversial. Here, we tested the hypothesis that stimulus representation persists in the frontal cortex to facilitate flexible control demands in WM. During functional MRI, participants flexibly switched between simple WM maintenance of visual stimulus or more complex rule-based categorization of maintained stimulus on a trial-by-trial basis. Our results demonstrated enhanced stimulus representation in the frontal cortex that tracked demands for active WM control and enhanced stimulus representation in the visual cortex that tracked demands for precise WM maintenance. This differential frontal stimulus representation traded off with the newly-generated category representation with varying control demands. Simulation using multi-module recurrent neural networks replicated human neural patterns when stimulus information was preserved for network readout. Altogether, these findings help reconcile the long-standing debate in WM research, and provide empirical and computational evidence that flexible stimulus representation in the frontal cortex during WM serves as a potential neural coding scheme to accommodate the ever-changing environment.
