Age-Dependent Modulations of Resting State Connectivity Following Motor Practice

Elena Solesio-Jofre, Iseult A M Beets, Daniel G Woolley, Lisa Pauwels, Sima Chalavi, Dante Mantini, Stephan P Swinnen, Elena Solesio-Jofre, Iseult A M Beets, Daniel G Woolley, Lisa Pauwels, Sima Chalavi, Dante Mantini, Stephan P Swinnen

Abstract

Recent work in young adults has demonstrated that motor learning can modulate resting state functional connectivity. However, evidence for older adults is scarce. Here, we investigated whether learning a bimanual tracking task modulates resting state functional connectivity of both inter- and intra-hemispheric regions differentially in young and older individuals, and whether this has behavioral relevance. Both age groups learned a set of complex bimanual tracking task variants over a 2-week training period. Resting-state and task-related functional magnetic resonance imaging scans were collected before and after training. Our analyses revealed that both young and older adults reached considerable performance gains. Older adults even obtained larger training-induced improvements relative to baseline, but their overall performance levels were lower than in young adults. Short-term practice resulted in a modulation of resting state functional connectivity, leading to connectivity increases in young adults, but connectivity decreases in older adults. This pattern of age differences occurred for both inter- and intra-hemispheric connections related to the motor network. Additionally, long-term training-induced increases were observed in intra-hemispheric connectivity in the right hemisphere across both age groups. Overall, at the individual level, the long-term changes in inter-hemispheric connectivity correlated with training-induced motor improvement. Our findings confirm that short-term task practice shapes spontaneous brain activity differentially in young and older individuals. Importantly, the association between changes in resting state functional connectivity and improvements in motor performance at the individual level may be indicative of how training shapes the short-term functional reorganization of the resting state motor network for improvement of behavioral performance.

Keywords: aging; bimanual coordination; motor learning; motor network; resting state functional connectivity.

Figures

FIGURE 1
FIGURE 1
Experimental setup and task. (A) Schematic representation of the experimental setup. Two scan sessions occurred before (pre-test session) and after (post-test session) five training sessions (training period), distributed across 2 weeks. Each scan session included a rest scan (rs1 and rs3, respectively) before a task-related scan, a task-related scan (tr1 and tr2, respectively) and a rest scan after the task-related scan (rs2 and rs4, respectively). We mainly focused on rest scans (i.e., two runs within each scan session, four runs in total: rs1, rs2, rs3, and rs4); (B) The goal of the bimanual tracking task was to track a white target dot over a blue target line, presented on a screen, by rotating two dials with both hands simultaneously in one of four directional patterns: inward (IN), outward (OUT), clockwise (CW), and counter-clockwise manner (CCW); at five different relative frequency ratios: 1:1, 1:2, 1:3, 2:1, and 3:1 (left: right). This resulted in 20 different bimanual patterns and target line directions.
FIGURE 2
FIGURE 2
Selected ROIs in the motor network. Spherical ROIs were defined bilaterally for the following areas: SMA, supplementary motor area; PMd, dorsal premotor area; M1, primary motor cortex; S1, primary somatosensory area; PMv, ventral premotor area. The ROIs are illustrated over a cortical representation for the right hemisphere only.
FIGURE 3
FIGURE 3
Brain-behavior correlations. (A) Functional connectivity measures: Connectivity changes extracted from rs2 minus rs1 (FC short-term learning), and also from rs4 minus rs1 (FC long-term learning) for inter- (homotopic, heterotopic) and intra-hemispheric (right, left) connectivity measures. (B) BTT gain measures: Last 15 trials of tr1 minus first 15 trials of tr1 (BTT Gain 1), and also last 15 trials of tr2 minus first 15 trials of tr1 (BTT Gain 2) for N-ISO conditions.
FIGURE 4
FIGURE 4
Behavioral performance during the scan and training sessions for the N-ISO condition. There was an initial reduction in target deviation error during the pre-test session, indicative of initial learning. During the training period, BTT performance became more stable, particularly during the last two training days. YA showed a more stable performance during the post-test session than OA, especially in the most difficult task condition (N-ISO). Error bars represent the standard error of the mean (SEM). N-ISO, non-isofrequency.
FIGURE 5
FIGURE 5
Correlation matrices across all participants showing the strength of functional connectivity between each pair of regions from the motor network for the four rest scans collected in the present study. Significant correlations (Bonferroni corrected probability, p < 0.001) are indicated with a black dot. Color bar on the right indicates t-values.
FIGURE 6
FIGURE 6
Bar plots showing the age × scan location interaction effect for inter-hemispheric functional connectivity. (A) Changes in connectivity in homotopic pairs of regions. (B) Changes in connectivity in heterotopic pairs of regions. In both cases, functional connectivity increased after task performance in YA, whereas it decreased in OA and we observed this pattern of results within both the pre- and post-test sessions. Moreover, homotopic functional connectivity was greater than heterotopic functional connectivity. Error bars represent SEM. Hm rs1+rs3, homotopic rest scans before task-related scans; Hm rs2+rs4, homotopic rest scans after task-related scans; Ht rs1+rs3, heterotopic rest scans before task-related scans; Ht rs2+rs4, heterotopic rest scans after task-related scans.
FIGURE 7
FIGURE 7
Bar plots show the age × scan location interaction effect for intra-hemispheric functional connectivity. (A) Changes in connectivity in right hemisphere pairs of regions. (B) Changes in connectivity in left hemisphere pairs of regions. In both cases, functional connectivity increased after task performance in YA, whereas it decreased after task performance in OA within pre- and post-test sessions. Error bars represent SEM.
FIGURE 8
FIGURE 8
Brain connectivity-behavior correlation. Scatter plot representing the significant correlation surviving Bonferroni correction (p < 0.025) between rs-FC change (y-axis) and bimanual coordination gain (x-axis). r, Pearson coefficient.

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