A combined diffusion-weighted and electroencephalography study on age-related differences in connectivity in the motor network during bimanual performance

Abstract

We studied the relationship between age-related differences in inter- and intra-hemispheric structural and functional connectivity in the bilateral motor network. Our focus was on the correlation between connectivity and declined motor performance in older adults. Structural and functional connectivity were estimated using diffusion weighted imaging and resting-state electro-encephalography, respectively. A total of 48 young and older healthy participants were measured. In addition, motor performances were assessed using bimanual coordination tasks. To pre-select regions-of-interest (ROIs), a neural model was adopted that accounts for intra-hemispheric functional connectivity between dorsal premotor area (PMd) and primary motor cortex (M1) and inter-hemispheric connections between left and right M1 (M1_L and M1_R ). Functional connectivity was determined via the weighted phase-lag index (wPLI) in the source-reconstructed beta activity during rest. We quantified structural connectivity using kurtosis anisotropy (KA) values of tracts derived from diffusion tensor-based fiber tractography between the aforementioned areas. In the group of older adults, wPLI values between M1_L -M1_R were negatively associated with the quality of bimanual motor performance. The additional association between wPLI values of PMd_L --M1_L and PMd_R -M1_L supports that functional connectivity with the left hemisphere mediated (bimanual) motor control in older adults. The correlational analysis between the selected structural and functional connections revealed a strong association between wPLI values in the left intra-hemispheric PMd_L -M1_L pathway and KA values in M1_L -M1_R and PMd_R -M1_L pathways in the group of older adults. This suggests that weaker structural connections in older adults correlate with stronger functional connectivity and, hence, poorer motor performance.

Keywords: DWI; EEG; aging; bimanual coordination; functional connectivity; motor control; structural connectivity.

Figure 1

Illustration of the motor task. Participants were asked to rotate two disks (left/right) to move a cursor visible after execution of the movement. A particular ratio of rotational frequency yielded movement along a prescribed line. The direction of the line discriminated three different frequency ratios. During execution of the tasks (8 s) no online feedback was provided (left panel). After every trial, feedback of the performance was displayed as shown for 2 s (right panel) [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 2

The panels illustrate the bimanual performance in three tasks with 1:1, 2:5, and 5:2 ratios. (a) Radial trajectories of wrist rotations. (b) Cross‐spectral overlap Ψ of trials across different p‐values. Dashed lines indicate the window of target ratio. The average value in this window served as a measure of performance. (c) Averaged measures of performance across five trials per task creating one block in one young participant. Participants executed the task in three blocks. Data are from the retention test [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 3

The selected regions‐of‐interest (ROIs) and their connections according to the model of functional connectivity by Daffertshofer et al. (2005) [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 4

Two examples of the extracted tracts between PMd_R and M1_R. Upper row: A younger participant, lower row: An older participant. The tracts are displayed on the participant's T1 image. Colors represent FA values, ranged from 0 to 1; A: Anterior, P: Posterior, R: Right, L: Left [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 5

Mean level of the spectral overlap Ψ for each movement frequency ratio in young and older adults. Older adults showed worse performance than younger adults across all frequency ratios, that is, behavioral tasks, as reflected by a smaller spectral overlap. However, not all ratios yielded significant differences. Error bars indicate the 95% CI; * indicates significant effects with p < 0.05 and *** p < 0.001 [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 6

KA values in younger and older adults. KA values were significantly lower in older adults than younger adults across all pathways of interest. Post‐hoc tests revealed that only the KA‐values of PMd_R–M1_R was significantly decreased in the older adults. Error bars indicate the 95% CI; ** indicates significant effects with p < 0.01, **** p < 10⁻⁴ [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 7

Functional connectivity (wPLI) between pairs of cortical regions in young and older adults. The wPLI value of PMd_L–M1_L was significantly increased in older adults. Error bars indicate the 95% CI; * indicates significant effects with p < 0.05 [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 8

Scatter plots of bimanual performance (Ψ) versus wPLI and KA. Left panel: Increased structural connectivity between PM1_R–M1_L was significantly associated with less coordinated bimanual performance in 1:1 ratio within the young group. Right panel: Increased functional coupling between M1_L–M1_R was significantly associated with less coordinated bimanual performance in 5:2 ratio within the group of older adults [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 9

Scatter plot representing the significant relationship between intra‐hemispheric and inter‐hemispheric functional couplings. Only in older adults, greater wPLI value of PMd_L–M1_L was associated with higher wPLI value of PMd_R–M1_R [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 10

Scatter plots representing intra‐hemispheric wPLI versus KA values. Left panel: Only in the older adults, larger wPLI values of PMd_L–M1_L were associated with lower KA values of M1_L–M1_R and PMd_R–M1_L (right panel) [Color figure can be viewed at http://wileyonlinelibrary.com]