Short-term plasticity following motor sequence learning revealed by diffusion magnetic resonance imaging

Abstract

Current noninvasive methods to detect structural plasticity in humans are mainly used to study long-term changes. Diffusion magnetic resonance imaging (MRI) was recently proposed as a novel approach to reveal gray matter changes following spatial navigation learning and object-location memory tasks. In the present work, we used diffusion MRI to investigate the short-term neuroplasticity that accompanies motor sequence learning. Following a 45-min training session in which participants learned to accurately play a short sequence on a piano keyboard, changes in diffusion properties were revealed mainly in motor system regions such as the premotor cortex and cerebellum. In a second learning session taking place immediately afterward, feedback was given on the timing of key pressing instead of accuracy, while participants continued to learn. This second session induced a different plasticity pattern, demonstrating the dynamic nature of learning-induced plasticity, formerly thought to require months of training in order to be detectable. These results provide us with an important reminder that the brain is an extremely dynamic structure. Furthermore, diffusion MRI offers a novel measure to follow tissue plasticity particularly over short timescales, allowing new insights into the dynamics of structural brain plasticity.

Keywords: diffusion MRI; learning; motor; neuroplasticity; piano.

© 2019 The Authors. Human Brain Mapping published by Wiley Periodicals, Inc.

Figures

Figure 1

Performance in piano training (Session 1). Accuracy of key pressing during the first learning session is shown by the absolute number of correct notes (a) and the normalized accuracy levels (b). Blue circles represent the average number of correct notes played by participants in each trial. The number of notes that were presented to participants in each trial is shown in red. On average, the best performance participants achieved was 46.6 correct notes out of 51. Error bars depict SEM [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 2

Performance in piano training (Session 2). Accuracy in the timing of key pressing during the first (a) and second (b) learning sessions is shown. Blue circles represent the average error in time per note for each trial. (a) During the first learning session, subjects did not show a decrease in their error rate. Red arrows indicate trials in which the number of notes increased. (b) During the second learning session, subjects' error rate decreased dramatically as they reached to an average error per note shorter than 20 ms. Error bars depict SEM [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 3

Reduction in mean diffusivity after piano training (Session 1). Structural remodeling of brain tissue, measured by DTI as a reduction in mean diffusivity (MD) after 45 min of training on a motor sequence learning task. A paired t test between the MD maps before and after the learning task (first session) was performed. The statistical parametric map is presented superimposed on coronal (upper row) and axial (lower row) slices of a single‐subject T1 map. Significant clusters of MD decrease were found in the left premotor cortex, left middle temporal gyrus and the cerebellum (p < .005, cluster size >37, equivalent to p < .05, corrected for multiple comparisons). L indicates the left side of the brain; color bar represents the T value [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 4

Reduction in mean diffusivity (a) after piano training (Session 2) and (b) after professional pianists' exposure to the task. Structural remodeling of brain tissue, measured by DTI as a reduction in mean diffusivity (MD) after 45 min of training on a motor sequence learning task. (a) In a second training session in the naïve participants feedback was given on the timing of key pressing. Analysis of variance (ANOVA) of the MD maps before and after each learning task was performed, and post hoc analysis revealed a significant cluster in the left lingual gyrus (p < .005, cluster size >37, equivalent to p < .05, corrected for multiple comparisons) in which the effect was a result of a reduction in MD after the second learning session. (b) Professional pianists experienced a piano‐playing session similar to the first session in the naïve participants. A paired t test between the MD maps before and after the session was performed. Significant clusters of MD decrease were found in the primary motor cortex bilaterally and in the ventromedial prefrontal cortex (vmPFC). p < .005, cluster size >37, equivalent to p < .05, corrected for multiple comparisons. The statistical parametric maps are presented superimposed on coronal (upper row) and axial (lower row) slices of a single‐subject T1 map. L indicates the left side of the brain; color bar represents the statistic (F or T) value [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 5

Specificity of brain networks plasticity to the learning procedure. Significant reduction in mean diffusivity was found in different brain regions for different stages of learning. Regions that underwent significant change after the first training session, in which feedback was given on accuracy, are presented on the left; regions of significant change after the second training session, in which feedback was given on timing, are presented in the middle; regions that were found in professional pianists are presented on the right. For each of these regions, the percentage reduction in mean diffusivity ([MD after–MD before]/MD before) is shown for three conditions: accuracy and timing training of naïve subjects (blue and red bars, respectively) and training of the professional pianists (green bar). The first scan was used as baseline for all conditions. The values presented refer to the MD decrease within the significant clusters. Error bars depict the SEM [Color figure can be viewed at http://wileyonlinelibrary.com]