Learning-related contraction of gray matter in rodent sensorimotor cortex is associated with adaptive myelination
From observations in rodents, it has been suggested that the cellular basis of learning-dependent changes, detected using structural MRI, may be increased dendritic spine density, alterations in astrocyte volume, and adaptations within intracortical myelin. Myelin plasticity is crucial for neurologi...
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2022-11-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/77432 |
| _version_ | 1811319164115091456 |
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| author | Tomas Mediavilla Özgün Özalay Héctor M Estévez-Silva Bárbara Frias Greger Orädd Fahad R Sultan Claudio Brozzoli Benjamín Garzón Martin Lövdén Daniel J Marcellino |
| author_facet | Tomas Mediavilla Özgün Özalay Héctor M Estévez-Silva Bárbara Frias Greger Orädd Fahad R Sultan Claudio Brozzoli Benjamín Garzón Martin Lövdén Daniel J Marcellino |
| author_sort | Tomas Mediavilla |
| collection | DOAJ |
| description | From observations in rodents, it has been suggested that the cellular basis of learning-dependent changes, detected using structural 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 nonlinear decreases in gray matter volume (GMV) juxtaposed to nonlinear increases in white matter volume (WMV) within GM that were best modeled by an asymptotic time course. Using an atlas-based cortical mask, we found nonlinear 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 nonlinear 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 nonlinear increase of intracortical myelin during learning and support the hypothesis that myelin is a component of structural changes observed by VBM during learning. |
| first_indexed | 2024-04-13T12:38:19Z |
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| id | doaj.art-9156eff25b38432bbe523f34e734a5a3 |
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| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-13T12:38:19Z |
| publishDate | 2022-11-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-9156eff25b38432bbe523f34e734a5a32022-12-22T02:46:36ZengeLife Sciences Publications LtdeLife2050-084X2022-11-011110.7554/eLife.77432Learning-related contraction of gray matter in rodent sensorimotor cortex is associated with adaptive myelinationTomas Mediavilla0Özgün Özalay1Héctor M Estévez-Silva2Bárbara Frias3Greger Orädd4Fahad R Sultan5Claudio Brozzoli6Benjamín Garzón7Martin Lövdén8Daniel J Marcellino9https://orcid.org/0000-0002-4618-7267Department of Integrative Medical Biology, Umeå University, Umeå, SwedenDepartment of Integrative Medical Biology, Umeå University, Umeå, SwedenDepartment of Integrative Medical Biology, Umeå University, Umeå, SwedenDepartment of Integrative Medical Biology, Umeå University, Umeå, SwedenDepartment of Integrative Medical Biology, Umeå University, Umeå, SwedenDepartment of Integrative Medical Biology, Umeå University, Umeå, SwedenIMPACT, Centre de Recherche en Neurosciences de Lyon, Lyon, France; Aging Research Center, Department of Neurobiology, Care Sciences and Society, Karolinska Institute, Solna, SwedenAging Research Center, Department of Neurobiology, Care Sciences and Society, Karolinska Institute, Solna, Sweden; Department of Psychology, University of Gothenburg, Gothenburg, SwedenAging Research Center, Department of Neurobiology, Care Sciences and Society, Karolinska Institute, Solna, Sweden; Department of Psychology, University of Gothenburg, Gothenburg, SwedenDepartment of Integrative Medical Biology, Umeå University, Umeå, SwedenFrom observations in rodents, it has been suggested that the cellular basis of learning-dependent changes, detected using structural 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 nonlinear decreases in gray matter volume (GMV) juxtaposed to nonlinear increases in white matter volume (WMV) within GM that were best modeled by an asymptotic time course. Using an atlas-based cortical mask, we found nonlinear 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 nonlinear 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 nonlinear increase of intracortical myelin during learning and support the hypothesis that myelin is a component of structural changes observed by VBM during learning.https://elifesciences.org/articles/77432VBMmotor skill learningMRImyelin |
| spellingShingle | Tomas Mediavilla Özgün Özalay Héctor M Estévez-Silva Bárbara Frias Greger Orädd Fahad R Sultan Claudio Brozzoli Benjamín Garzón Martin Lövdén Daniel J Marcellino Learning-related contraction of gray matter in rodent sensorimotor cortex is associated with adaptive myelination eLife VBM motor skill learning MRI myelin |
| title | Learning-related contraction of gray matter in rodent sensorimotor cortex is associated with adaptive myelination |
| title_full | Learning-related contraction of gray matter in rodent sensorimotor cortex is associated with adaptive myelination |
| title_fullStr | Learning-related contraction of gray matter in rodent sensorimotor cortex is associated with adaptive myelination |
| title_full_unstemmed | Learning-related contraction of gray matter in rodent sensorimotor cortex is associated with adaptive myelination |
| title_short | Learning-related contraction of gray matter in rodent sensorimotor cortex is associated with adaptive myelination |
| title_sort | learning related contraction of gray matter in rodent sensorimotor cortex is associated with adaptive myelination |
| topic | VBM motor skill learning MRI myelin |
| url | https://elifesciences.org/articles/77432 |
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