Dynamic properties of human brain structure: learning-related changes in cortical areas and associated fiber connections

Abstract

Recent findings in neuroscience suggest that adult brain structure changes in response to environmental alterations and skill learning. Whereas much is known about structural changes after intensive practice for several months, little is known about the effects of single practice sessions on macroscopic brain structure and about progressive (dynamic) morphological alterations relative to improved task proficiency during learning for several weeks. Using T1-weighted and diffusion tensor imaging in humans, we demonstrate significant gray matter volume increases in frontal and parietal brain areas following only two sessions of practice in a complex whole-body balancing task. Gray matter volume increase in the prefrontal cortex correlated positively with subject's performance improvements during a 6 week learning period. Furthermore, we found that microstructural changes of fractional anisotropy in corresponding white matter regions followed the same temporal dynamic in relation to task performance. The results make clear how marginal alterations in our ever changing environment affect adult brain structure and elucidate the interrelated reorganization in cortical areas and associated fiber connections in correlation with improvements in task performance.

Figures

Figure 1.

Experimental design and behavioral and electrophysiological results. A, Experimental design. Subjects performed 15 trials (∼45 min) of the whole-body DBT on each of the six TDs as well as in the retention test (RT) and received verbal feedback about their performance after each trial (see below). Before the learning session on TD1, TD3, TD5, and in the seventh week, structural MRI scans were performed to assess learning-related gray and white matter changes. B, DBT. Subjects were instructed to keep a balance platform in a horizontal position as long as possible during a trial length of 30 s. Motor performance was determined as the time {s) in which the subjects kept the platform in a horizontal position, within a deviation range of ± 3° to each side, out of the total trial length of 30 s (BAL). C, Behavioral results. Improvements in motor performance during the time course of learning as well as mean retention performance of 95% (in percentage of mean performance on TD6) after 3 months without training (filled squares, mean performance across subjects; error bars, SEM). Asterisks indicate significant improvements in motor performance between consecutive training days (TD1 to TD2, p < 0.001, TD2 to TD3, p < 0.001; TD4 to TD5, p < 0.001; see also Fig. S1, available at www.jneurosci.org as supplemental material, for within-session improvements). D, Negative correlation between muscular imbalances and motor performance during the learning period (dotted lines indicate SD for muscular imbalances and motor performance; see also Fig. S2, available at www.jneurosci.org as supplemental material).

Figure 2.

Increase in GM volume and decrease in WM FA across the whole learning period (s1–s2, s3, s4). These analyses are independent from improvements in motor performance. GM (yellow) and WM (cyan) changes in bilateral lateral prefrontal regions are shown in axial sections overlaid on MNI colin27 image (top image) and individual (normalized) FA map (bottom image). Images are shown at p < 0.05 (corrected). Bars indicate t values. R, Right; L, left; P, posterior; A, anterior.

Figure 3.

A, Rapid changes in GM volume and WM FA from s1–s2 (paired t test). Rendered brains indicate GM expansion (yellow) and FA decrease (cyan). Top image shows left side of the brain. Upper two coronal sections show GM expansion in bilateral lateral prefrontal cortex. Middle coronal section shows FA decrease in left prefrontal WM. Bottom left section indicates GM expansion in bilateral supplementary motor areas. B, Positive linear correlation between GM expansion in left supplementary motor areas and individual adaptations in muscular imbalances across the whole learning period (Fig. S3, available at www.jneurosci.org as supplemental material). GM and WM changes are shown in coronal sections overlaid on MNI colin27 image and individual (normalized) FA map. All images are shown at p < 0.05 (corrected). Bars indicate t values. R, Right; L, left; P, posterior; A, anterior.

Figure 4.

Parametric correlation between individual improvements in motor performance across the whole learning period (s1, s2, s3, and s4) and GM volume and WM, FA and MD. A, Positive linear correlation between improvements in motor performance and GM expansion in left sOFC. GM changes are shown in axial section (red dotted circle). B, Negative linear correlation between improvements in motor performance and FA changes in left prefrontal and right parietal WM regions (cyan). Right rendered brain represents right hemisphere. FA changes are shown in axial sections. C, Negative linear correlation between improvements in motor performance and MD changes in bilateral anterior centrum semiovale, left brainstem and right internal capsule (cyan). All images are shown at p < 0.05 (corrected). Bars indicate t values. R, Right; L, left; P, posterior; A, anterior.

Figure 5.

Temporal dynamics of GM and WM FA and MD changes during learning. A, GM. Diagram shows percentage signal change (error bars indicate SEM) on s2, s3, and s4 relative to baseline (s1) in peak voxel in left OFC, SFG, and SMA. B, WM. Diagram shows percentage signal change (error bars indicate SEM) in FA/MD during learning in peak voxel in WM regions adjoining left OFC and in left anterior centrum semiovale. Asterisks indicate significant changes in peak voxel intensity compared to baseline (s1) intensity at p < 0.05 (paired t test).