Aging and Complexity Effects on Hemisphere-Dependent Movement-Related Beta Desynchronization during Bimanual Motor Planning and Execution

Abstract

With aging comes degradation of bimanual movement performance. A hallmark feature of bimanual movements is movement-related beta desynchronization (MRBD), an attenuation in the amplitude of beta oscillations associated with sensorimotor activation. Here, we investigated MRBD in 39 healthy adults (20 younger and 19 older adults) in frontal, central, and parietal regions across both hemispheres, during the planning and execution of a bimanual tracking task. Task accuracy decreased with age and during more difficult conditions when both hands had to move at different relative speeds. MRBD was mostly situated in the central region, and increased in older versus younger adults during movement execution but not planning. Irrespective of age, motor planning and execution were associated with increased MRBD in the left and right hemispheres, respectively. Notably, right central MRBD during motor planning was associated with bimanual task performance, particularly in older adults. Specifically, persons who demonstrated high MRBD during motor planning performed better on the bimanual tracking task. Our results highlight the importance of lateralized MRBD during motor planning, thereby shining new light on previous research and providing a promising avenue for future interventions.

Keywords: aging; beta oscillations; bimanual coordination; electroencephalography; interlimb coordination; motor execution; motor planning; time-frequency analysis.

Figure A1

Grand-average time-frequency mask obtained by averaging the power values per time- and frequency-point, across all participants, electrodes and BTT conditions. This mask was used for power value extraction. Specifically, the mean beta power value within the black contours was extracted per participant, electrode and BTT condition and used in the statistical analyses. The black contours were defined by a statistical masking procedure (cf., Section 2.5.2. Effect of age, hemispheric laterality, and complexity on MRBD during bimanual planning and execution (Hypotheses 2–4)). Colors denote spectral power, with dark blue and red being −3 and 3 dB, respectively.

Figure A2

Violin plots of beta power per stage, condition, region, and hemisphere. Lower power values denote higher movement-related beta desynchronization.

Figure A3

Interaction profile plot for effect of complexity on beta power during movement planning, irrespective of laterality. This plot was made for the sake of comparability with previous research. Black lines denote significant contrasts (p < 0.050), gray lines denote marginally significant contrasts (p = 0.079).

Figure 1

Bimanual tracking task. (A). Task set-up. (B). Task conditions, with 1:1 denoting an identical relative inter-hand frequency, and 3:1 and 1:3 denoting that the left or right hand, respectively, rotated three times faster than the other hand. (C). Time course of a 1:1 trial. The red and black dots denote the target and participant’s cursor location, respectively. The blue line supplies feedback about the completed trajectory.

Figure 2

Performance on bimanual tracking task. The tracking error represents compliancy with the imposed movement condition, with a lower value representing better performance. (A). Box- and violin plots showing tracking error distribution per age group and condition. Whisker length is 1.5 × interquartile value. (B). Effect of condition on tracking error. (C). Effect of group on tracking error. Errors bars in (B,C) denote 95% confidence intervals, horizontal black lines denote significant post-hoc contrasts.

Figure 3

Time-frequency plots per group, condition, region, and hemisphere. The y-axis displays frequency (3–35 Hz), the x-axis displays time (−2.5–3.5 s), and the color scale displays power (−7–7 dB), with blue colors in the beta-range (13–30 Hz) reflecting movement-related beta desynchronization. Vertical dashed lines denote onset of the planning (−2 s) and execution stage (0 s).

Figure 4

Topographic plots of spectral beta activity during rest, motor planning and execution in both older and younger adults for all three task conditions. The color scaling displays power (−7–7 dB), with blue colors reflecting movement-related beta desynchronization.

Figure 5

Interaction plots for movement-related beta desynchronization (MRBD) during motor planning. Lower power values represent more MRBD. In line with Hypothesis 3, MRBD was more prevalent in the left hemisphere. Notably, no hemisphere×group effect was present, contrary to Hypothesis 4. Error bars denote the 95% confidence interval, horizontal lines denote significant post-hoc contrasts with colors indicating within hemisphere/group differences and black lines indicating hemisphere / group differences.

Figure 6

Interaction plots for movement-related beta desynchronization (MRBD) during motor execution. Lower values represent more MRBD. MRBD was higher in older adults, consistent with Hypothesis 2. Partially in line with Hypothesis 3, MRBD was higher in the frontal and central right versus left regions in older adults. Opposed to Hypothesis 4, hemispheric laterality was only present in older adults. Error bars display the 95% confidence interval. Horizontal lines denote significant contrasts with colored and black lines indicating within-group and between-group differences, respectively. Between-hemisphere significant contrasts are visualized brighter than between-region contrasts.

Figure 7

Functional role of movement-related beta desynchronization (MRBD). (A). Correlation between central right motor planning MRBD and tracking error. Better performance (lower error) is associated with higher MRBD. The black line shows the average correlation (ρ = 0.49, p = 0.002), the blue and red lines show the correlations for younger (ρ = 0.14, p = 0.551) and older adults (ρ = 0.56, p = 0.014). (B). Absolute central power (post-Laplacian transformation), during the bimanual tracking task (BTT). This figure aids mechanistic understanding of MRBD. Here, MRBD is the reduction of beta power at a specific timepoint during motor planning or motor execution, relative to beta power during rest.