Gray matter volume is associated with rate of subsequent skill learning after a long term training intervention
Cassandra Sampaio-Baptista, Jan Scholz, Mark Jenkinson, Adam G Thomas, Nicola Filippini, Gabrielle Smit, Gwenaëlle Douaud, Heidi Johansen-Berg, Cassandra Sampaio-Baptista, Jan Scholz, Mark Jenkinson, Adam G Thomas, Nicola Filippini, Gabrielle Smit, Gwenaëlle Douaud, Heidi Johansen-Berg
Abstract
The ability to predict learning performance from brain imaging data has implications for selecting individuals for training or rehabilitation interventions. Here, we used structural MRI to test whether baseline variations in gray matter (GM) volume correlated with subsequent performance after a long-term training of a complex whole-body task. 44 naïve participants were scanned before undertaking daily juggling practice for 6weeks, following either a high intensity or a low intensity training regime. To assess performance across the training period participants' practice sessions were filmed. Greater GM volume in medial occipito-parietal areas at baseline correlated with steeper learning slopes. We also tested whether practice time or performance outcomes modulated the degree of structural brain change detected between the baseline scan and additional scans performed immediately after training and following a further 4weeks without training. Participants with better performance had higher increases in GM volume during the period following training (i.e., between scans 2 and 3) in dorsal parietal cortex and M1. When contrasting brain changes between the practice intensity groups, we did not find any straightforward effects of practice time though practice modulated the relationship between performance and GM volume change in dorsolateral prefrontal cortex. These results suggest that practice time and performance modulate the degree of structural brain change evoked by long-term training regimes.
Keywords: MRI; Skill learning; Structural plasticity.
Copyright © 2014. Published by Elsevier Inc.
Figures
![Fig. S1](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/4075341/bin/gr6.jpg)
![Fig. 1](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/4075341/bin/gr1.jpg)
![Fig. 2](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/4075341/bin/gr2.jpg)
Fig. 3
Interaction effect between practice group…
Fig. 3
Interaction effect between practice group and average performance, between scan 1 and scan…
Fig. 4
Longer term effects: Scans 1…
Fig. 4
Longer term effects: Scans 1 to 3 and scans 2 to 3. a)…
Fig. 5
Participants with better performance have…
Fig. 5
Participants with better performance have higher GM increases during the follow-up period. a)…
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- Action observation training modifies brain gray matter structure in healthy adult individuals.Rocca MA, Fumagalli S, Pagani E, Gatti R, Riccitelli GC, Preziosa P, Comi G, Falini A, Filippi M. Rocca MA, et al. Brain Imaging Behav. 2017 Oct;11(5):1343-1352. doi: 10.1007/s11682-016-9625-3. Brain Imaging Behav. 2017. PMID: 27730478 Clinical Trial.
- Dynamic gray matter changes within cortex and striatum after short motor skill training are associated with their increased functional interaction.Hamzei F, Glauche V, Schwarzwald R, May A. Hamzei F, et al. Neuroimage. 2012 Feb 15;59(4):3364-72. doi: 10.1016/j.neuroimage.2011.10.089. Epub 2011 Nov 12. Neuroimage. 2012. PMID: 22108643
- Expansion and Renormalization of Human Brain Structure During Skill Acquisition.Wenger E, Brozzoli C, Lindenberger U, Lövdén M. Wenger E, et al. Trends Cogn Sci. 2017 Dec;21(12):930-939. doi: 10.1016/j.tics.2017.09.008. Trends Cogn Sci. 2017. PMID: 29149999 Free PMC article. Review.
- Teaching an adult brain new tricks: a critical review of evidence for training-dependent structural plasticity in humans.Thomas C, Baker CI. Thomas C, et al. Neuroimage. 2013 Jun;73:225-36. doi: 10.1016/j.neuroimage.2012.03.069. Epub 2012 Mar 30. Neuroimage. 2013. PMID: 22484409 Review.
- Twelve Weeks of Web-Based Low to Moderate Physical Activity Breaks with Coordinative Exercises at the Workplace Increase Motor Skills but Not Motor Abilities in Office Workers-A Randomised Controlled Pilot Study.Scharf C, Tilp M. Scharf C, et al. Int J Environ Res Public Health. 2023 Jan 25;20(3):2193. doi: 10.3390/ijerph20032193. Int J Environ Res Public Health. 2023. PMID: 36767561 Free PMC article. Clinical Trial.
- Effect of the Juggling-Based Motor Learning Physical Activity on Well-Being in Elderly: A Pre-Post Study with a Special Training Protocol.Malik J, Maciaszek J. Malik J, et al. Healthcare (Basel). 2022 Dec 3;10(12):2442. doi: 10.3390/healthcare10122442. Healthcare (Basel). 2022. PMID: 36553966 Free PMC article.
- Using whole-brain diffusion tensor analysis to evaluate white matter structural correlates of delayed visuospatial memory and one-week motor skill retention in nondemented older adults: A preliminary study.Lingo VanGilder J, Bergamino M, Hooyman A, Fitzhugh MC, Rogalsky C, Stewart JC, Beeman SC, Schaefer SY. Lingo VanGilder J, et al. PLoS One. 2022 Sep 22;17(9):e0274955. doi: 10.1371/journal.pone.0274955. eCollection 2022. PLoS One. 2022. PMID: 36137126 Free PMC article.
- Cortical change after a 2-week novel robotic rehabilitation program in children with prior hemispherectomy: pilot imaging study.Hazany S, Mann D, Bagrodia N, Krafnick AJ, Chu R Jr, Shaw S, Clark K. Hazany S, et al. Childs Nerv Syst. 2023 Feb;39(2):443-449. doi: 10.1007/s00381-022-05664-8. Epub 2022 Sep 10. Childs Nerv Syst. 2023. PMID: 36085526
- The Effect of Juggling as Dual-Task Activity on Human Neuroplasticity: A Systematic Review.Malik J, Stemplewski R, Maciaszek J. Malik J, et al. Int J Environ Res Public Health. 2022 Jun 9;19(12):7102. doi: 10.3390/ijerph19127102. Int J Environ Res Public Health. 2022. PMID: 35742356 Free PMC article. Review.
-
- Anderson B.J., Li X., Alcantara A.A., Isaacs K.R., Black J.E., Greenough W.T. Glial hypertrophy is associated with synaptogenesis following motor-skill learning, but not with angiogenesis following exercise. Glia. 1994;11:73–80. - PubMed
-
- Andersson J., Jenkinson M., Smith S. FMRIB Centre; Oxford (UK): 2007. Non-Linear Optimisation FMRIB Technical Report TR07JA1.
-
- Andersson J., Jenkinson M., Smith S. FMRIB Centre; Oxford (UK): 2007. Non-Linear Registration, aka Spatial Normalisation FMRIB Technical Report TR07JA2.
- Randomized Controlled Trial
- Research Support, Non-U.S. Gov't
- Brain / cytology*
- Brain / physiology*
- Female
- Gray Matter / cytology*
- Gray Matter / physiology*
- Humans
- Imaging, Three-Dimensional / methods
- Learning / physiology*
- Longitudinal Studies
- Magnetic Resonance Imaging / methods
- Male
- Motor Skills / physiology*
- Neuronal Plasticity / physiology
- Physical Conditioning, Human / methods
- Prefrontal Cortex / physiology*
- Reproducibility of Results
- Sensitivity and Specificity
- Young Adult
- Full Text Sources
- Other Literature Sources
- Medical
NCBI Literature Resources
The PubMed wordmark and PubMed logo are registered trademarks of the U.S. Department of Health and Human Services (HHS). Unauthorized use of these marks is strictly prohibited.
National Library of Medicine
8600 Rockville Pike
Bethesda, MD 20894
![Fig. 3](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/4075341/bin/gr3.jpg)
Fig. 4
Longer term effects: Scans 1…
Fig. 4
Longer term effects: Scans 1 to 3 and scans 2 to 3. a)…
Fig. 5
Participants with better performance have…
Fig. 5
Participants with better performance have higher GM increases during the follow-up period. a)…
- Interindividual differences in gray and white matter properties are associated with early complex motor skill acquisition.Lehmann N, Tolentino-Castro JW, Kaminski E, Ragert P, Villringer A, Taubert M. Lehmann N, et al. Hum Brain Mapp. 2019 Oct 15;40(15):4316-4330. doi: 10.1002/hbm.24704. Epub 2019 Jul 1. Hum Brain Mapp. 2019. PMID: 31264300 Free PMC article.
- Action observation training modifies brain gray matter structure in healthy adult individuals.Rocca MA, Fumagalli S, Pagani E, Gatti R, Riccitelli GC, Preziosa P, Comi G, Falini A, Filippi M. Rocca MA, et al. Brain Imaging Behav. 2017 Oct;11(5):1343-1352. doi: 10.1007/s11682-016-9625-3. Brain Imaging Behav. 2017. PMID: 27730478 Clinical Trial.
- Dynamic gray matter changes within cortex and striatum after short motor skill training are associated with their increased functional interaction.Hamzei F, Glauche V, Schwarzwald R, May A. Hamzei F, et al. Neuroimage. 2012 Feb 15;59(4):3364-72. doi: 10.1016/j.neuroimage.2011.10.089. Epub 2011 Nov 12. Neuroimage. 2012. PMID: 22108643
- Expansion and Renormalization of Human Brain Structure During Skill Acquisition.Wenger E, Brozzoli C, Lindenberger U, Lövdén M. Wenger E, et al. Trends Cogn Sci. 2017 Dec;21(12):930-939. doi: 10.1016/j.tics.2017.09.008. Trends Cogn Sci. 2017. PMID: 29149999 Free PMC article. Review.
- Teaching an adult brain new tricks: a critical review of evidence for training-dependent structural plasticity in humans.Thomas C, Baker CI. Thomas C, et al. Neuroimage. 2013 Jun;73:225-36. doi: 10.1016/j.neuroimage.2012.03.069. Epub 2012 Mar 30. Neuroimage. 2013. PMID: 22484409 Review.
- Twelve Weeks of Web-Based Low to Moderate Physical Activity Breaks with Coordinative Exercises at the Workplace Increase Motor Skills but Not Motor Abilities in Office Workers-A Randomised Controlled Pilot Study.Scharf C, Tilp M. Scharf C, et al. Int J Environ Res Public Health. 2023 Jan 25;20(3):2193. doi: 10.3390/ijerph20032193. Int J Environ Res Public Health. 2023. PMID: 36767561 Free PMC article. Clinical Trial.
- Effect of the Juggling-Based Motor Learning Physical Activity on Well-Being in Elderly: A Pre-Post Study with a Special Training Protocol.Malik J, Maciaszek J. Malik J, et al. Healthcare (Basel). 2022 Dec 3;10(12):2442. doi: 10.3390/healthcare10122442. Healthcare (Basel). 2022. PMID: 36553966 Free PMC article.
- Using whole-brain diffusion tensor analysis to evaluate white matter structural correlates of delayed visuospatial memory and one-week motor skill retention in nondemented older adults: A preliminary study.Lingo VanGilder J, Bergamino M, Hooyman A, Fitzhugh MC, Rogalsky C, Stewart JC, Beeman SC, Schaefer SY. Lingo VanGilder J, et al. PLoS One. 2022 Sep 22;17(9):e0274955. doi: 10.1371/journal.pone.0274955. eCollection 2022. PLoS One. 2022. PMID: 36137126 Free PMC article.
- Cortical change after a 2-week novel robotic rehabilitation program in children with prior hemispherectomy: pilot imaging study.Hazany S, Mann D, Bagrodia N, Krafnick AJ, Chu R Jr, Shaw S, Clark K. Hazany S, et al. Childs Nerv Syst. 2023 Feb;39(2):443-449. doi: 10.1007/s00381-022-05664-8. Epub 2022 Sep 10. Childs Nerv Syst. 2023. PMID: 36085526
- The Effect of Juggling as Dual-Task Activity on Human Neuroplasticity: A Systematic Review.Malik J, Stemplewski R, Maciaszek J. Malik J, et al. Int J Environ Res Public Health. 2022 Jun 9;19(12):7102. doi: 10.3390/ijerph19127102. Int J Environ Res Public Health. 2022. PMID: 35742356 Free PMC article. Review.
-
- Anderson B.J., Li X., Alcantara A.A., Isaacs K.R., Black J.E., Greenough W.T. Glial hypertrophy is associated with synaptogenesis following motor-skill learning, but not with angiogenesis following exercise. Glia. 1994;11:73–80. - PubMed
-
- Andersson J., Jenkinson M., Smith S. FMRIB Centre; Oxford (UK): 2007. Non-Linear Optimisation FMRIB Technical Report TR07JA1.
-
- Andersson J., Jenkinson M., Smith S. FMRIB Centre; Oxford (UK): 2007. Non-Linear Registration, aka Spatial Normalisation FMRIB Technical Report TR07JA2.
- Randomized Controlled Trial
- Research Support, Non-U.S. Gov't
- Brain / cytology*
- Brain / physiology*
- Female
- Gray Matter / cytology*
- Gray Matter / physiology*
- Humans
- Imaging, Three-Dimensional / methods
- Learning / physiology*
- Longitudinal Studies
- Magnetic Resonance Imaging / methods
- Male
- Motor Skills / physiology*
- Neuronal Plasticity / physiology
- Physical Conditioning, Human / methods
- Prefrontal Cortex / physiology*
- Reproducibility of Results
- Sensitivity and Specificity
- Young Adult
- Full Text Sources
- Other Literature Sources
- Medical
NCBI Literature Resources
The PubMed wordmark and PubMed logo are registered trademarks of the U.S. Department of Health and Human Services (HHS). Unauthorized use of these marks is strictly prohibited.
National Library of Medicine
8600 Rockville Pike
Bethesda, MD 20894
![Fig. 4](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/4075341/bin/gr4.jpg)
Fig. 5
Participants with better performance have…
Fig. 5
Participants with better performance have higher GM increases during the follow-up period. a)…
- Interindividual differences in gray and white matter properties are associated with early complex motor skill acquisition.Lehmann N, Tolentino-Castro JW, Kaminski E, Ragert P, Villringer A, Taubert M. Lehmann N, et al. Hum Brain Mapp. 2019 Oct 15;40(15):4316-4330. doi: 10.1002/hbm.24704. Epub 2019 Jul 1. Hum Brain Mapp. 2019. PMID: 31264300 Free PMC article.
- Action observation training modifies brain gray matter structure in healthy adult individuals.Rocca MA, Fumagalli S, Pagani E, Gatti R, Riccitelli GC, Preziosa P, Comi G, Falini A, Filippi M. Rocca MA, et al. Brain Imaging Behav. 2017 Oct;11(5):1343-1352. doi: 10.1007/s11682-016-9625-3. Brain Imaging Behav. 2017. PMID: 27730478 Clinical Trial.
- Dynamic gray matter changes within cortex and striatum after short motor skill training are associated with their increased functional interaction.Hamzei F, Glauche V, Schwarzwald R, May A. Hamzei F, et al. Neuroimage. 2012 Feb 15;59(4):3364-72. doi: 10.1016/j.neuroimage.2011.10.089. Epub 2011 Nov 12. Neuroimage. 2012. PMID: 22108643
- Expansion and Renormalization of Human Brain Structure During Skill Acquisition.Wenger E, Brozzoli C, Lindenberger U, Lövdén M. Wenger E, et al. Trends Cogn Sci. 2017 Dec;21(12):930-939. doi: 10.1016/j.tics.2017.09.008. Trends Cogn Sci. 2017. PMID: 29149999 Free PMC article. Review.
- Teaching an adult brain new tricks: a critical review of evidence for training-dependent structural plasticity in humans.Thomas C, Baker CI. Thomas C, et al. Neuroimage. 2013 Jun;73:225-36. doi: 10.1016/j.neuroimage.2012.03.069. Epub 2012 Mar 30. Neuroimage. 2013. PMID: 22484409 Review.
- Twelve Weeks of Web-Based Low to Moderate Physical Activity Breaks with Coordinative Exercises at the Workplace Increase Motor Skills but Not Motor Abilities in Office Workers-A Randomised Controlled Pilot Study.Scharf C, Tilp M. Scharf C, et al. Int J Environ Res Public Health. 2023 Jan 25;20(3):2193. doi: 10.3390/ijerph20032193. Int J Environ Res Public Health. 2023. PMID: 36767561 Free PMC article. Clinical Trial.
- Effect of the Juggling-Based Motor Learning Physical Activity on Well-Being in Elderly: A Pre-Post Study with a Special Training Protocol.Malik J, Maciaszek J. Malik J, et al. Healthcare (Basel). 2022 Dec 3;10(12):2442. doi: 10.3390/healthcare10122442. Healthcare (Basel). 2022. PMID: 36553966 Free PMC article.
- Using whole-brain diffusion tensor analysis to evaluate white matter structural correlates of delayed visuospatial memory and one-week motor skill retention in nondemented older adults: A preliminary study.Lingo VanGilder J, Bergamino M, Hooyman A, Fitzhugh MC, Rogalsky C, Stewart JC, Beeman SC, Schaefer SY. Lingo VanGilder J, et al. PLoS One. 2022 Sep 22;17(9):e0274955. doi: 10.1371/journal.pone.0274955. eCollection 2022. PLoS One. 2022. PMID: 36137126 Free PMC article.
- Cortical change after a 2-week novel robotic rehabilitation program in children with prior hemispherectomy: pilot imaging study.Hazany S, Mann D, Bagrodia N, Krafnick AJ, Chu R Jr, Shaw S, Clark K. Hazany S, et al. Childs Nerv Syst. 2023 Feb;39(2):443-449. doi: 10.1007/s00381-022-05664-8. Epub 2022 Sep 10. Childs Nerv Syst. 2023. PMID: 36085526
- The Effect of Juggling as Dual-Task Activity on Human Neuroplasticity: A Systematic Review.Malik J, Stemplewski R, Maciaszek J. Malik J, et al. Int J Environ Res Public Health. 2022 Jun 9;19(12):7102. doi: 10.3390/ijerph19127102. Int J Environ Res Public Health. 2022. PMID: 35742356 Free PMC article. Review.
-
- Anderson B.J., Li X., Alcantara A.A., Isaacs K.R., Black J.E., Greenough W.T. Glial hypertrophy is associated with synaptogenesis following motor-skill learning, but not with angiogenesis following exercise. Glia. 1994;11:73–80. - PubMed
-
- Andersson J., Jenkinson M., Smith S. FMRIB Centre; Oxford (UK): 2007. Non-Linear Optimisation FMRIB Technical Report TR07JA1.
-
- Andersson J., Jenkinson M., Smith S. FMRIB Centre; Oxford (UK): 2007. Non-Linear Registration, aka Spatial Normalisation FMRIB Technical Report TR07JA2.
- Randomized Controlled Trial
- Research Support, Non-U.S. Gov't
- Brain / cytology*
- Brain / physiology*
- Female
- Gray Matter / cytology*
- Gray Matter / physiology*
- Humans
- Imaging, Three-Dimensional / methods
- Learning / physiology*
- Longitudinal Studies
- Magnetic Resonance Imaging / methods
- Male
- Motor Skills / physiology*
- Neuronal Plasticity / physiology
- Physical Conditioning, Human / methods
- Prefrontal Cortex / physiology*
- Reproducibility of Results
- Sensitivity and Specificity
- Young Adult
- Full Text Sources
- Other Literature Sources
- Medical
![Fig. 5](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/4075341/bin/gr5.jpg)
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Source: PubMed