Effects of a 12-Week Aerobic Spin Intervention on Resting State Networks in Previously Sedentary Older Adults

Keith M McGregor, Bruce Crosson, Lisa C Krishnamurthy, Venkatagiri Krishnamurthy, Kyle Hortman, Kaundinya Gopinath, Kevin M Mammino, Javier Omar, Joe R Nocera, Keith M McGregor, Bruce Crosson, Lisa C Krishnamurthy, Venkatagiri Krishnamurthy, Kyle Hortman, Kaundinya Gopinath, Kevin M Mammino, Javier Omar, Joe R Nocera

Abstract

Objective: We have previously demonstrated that aerobic exercise improves upper extremity motor function concurrent with changes in motor cortical activity using task-based functional magnetic resonance imaging (fMRI). However, it is currently unknown how a 12-week aerobic exercise intervention affects resting-state functional connectivity (rsFC) in motor networks. Previous work has shown that over a 6-month or 1-year exercise intervention, older individuals show increased resting state connectivity of the default mode network and the sensorimotor network (Voss et al., 2010b; Flodin et al., 2017). However, the effects of shorter-term 12-week exercise interventions on functional connectivity have received less attention. Method: Thirty-seven sedentary right-handed older adults were randomized to either a 12-week aerobic, spin cycling exercise group or a 12-week balance-toning exercise group. Resting state functional magnetic resonance images were acquired in sessions PRE/POST interventions. We applied seed-based correlation analysis to left and right primary motor cortices (L-M1 and R-M1) and anterior default mode network (aDMN) to test changes in rsFC between groups after the intervention. In addition, we performed a regression analysis predicting connectivity changes PRE/POST intervention across all participants as a function of time spent in aerobic training zone regardless of group assignment. Results: Seeding from L-M1, we found that participants in the cycling group had a greater PRE/POST change in rsFC in aDMN as compared to the balance group. When accounting for time in aerobic HR zone, we found increased heart rate workload was positively associated with increased change of rsFC between motor networks and aDMN. Interestingly, L-M1 to aDMN connectivity changes were also related to motor behavior changes in both groups. Respective of M1 laterality, comparisons of all participants from PRE to POST showed a reduction in the extent of bilateral M1 connectivity after the interventions with increased connectivity in dominant M1. Conclusion: A 12-week physical activity intervention can change rsFC between primary motor regions and default mode network areas, which may be associated with improved motor performance. The decrease in connectivity between L-M1 and R-M1 post-intervention may represent a functional consolidation to the dominant M1. Topic Areas: Neuroimaging, Aging.

Keywords: aerobic exercise; aging; functional connectivity; motor control; resting state.

Figures

FIGURE 1
FIGURE 1
Study recruitment and participant flowchart. Of the 204 screened participants, 56 provided informed consent. Due to attrition or imaging artifacts, we report PRE/POST data from 37 participants (19 aerobic exercise; 18 balance training).
FIGURE 2
FIGURE 2
The changes in VO2 max were significantly different between AE and BAL groups, indicating the success of the aerobic spin intervention. The AE group also spent a greater amount of time in the prescribed Target HR Zone during their 12 weeks intervention, as indicated by the % Time in HR Target Zone.
FIGURE 3
FIGURE 3
Resulting rsfMRI connectivity maps from R-M1, L-M1, and aDMN seeds. The intensity of the connectivity maps represent T score, thresholded at p = 0.0001, cluster size = 100. The green lines overlaid on the sagittal image represent the location of the displayed axial slices.
FIGURE 4
FIGURE 4
The AE-BAL group t-test of Z(CC)DIFF seeded from L-M1 shows aDMN connectivity differences, indicating that the 12-week aerobic spin intervention was able to significantly L-M1 to aDMN connectivity in the AE group (p = 0.01, cluster size = 50). To further understand the relationship between individual subject response to the intervention, the % Time in Target HR Zone was correlated with Z(CC)DIFF seeded from L-M1 on a voxel-wise basis as described in Equation 4. The regression analysis also shows exercise induced changes in L-M1 to aDMN connectivity, along with L-M1 to pDMN, and L-M1 to L-PMd connectivity (p = 0.01, cluster size = 50). The plots show the average Z(CC)DIFF from the extracted ROI is predicted significantly by % Time in Target HR Zone. Closed circles = AE; Open circles = BAL.
FIGURE 5
FIGURE 5
The AE-BAL group t-test of Z(CC)DIFF seeded from aDMN shows L-M1 connectivity differences, which is expected based on the L-M1 seed results. However, when taking into account the individual subject response to the intervention by regressing Z(CC)DIFF with % Time in Target HR Zone, both aDMN to L-M1 and aDMN to R-M1 connectivity relationships became apparent. A bilateral aDMN to Precuneus connectivity relationship also emerged with the regression analysis. These results indicate the importance of taking into account the individual subject response to the intervention to ascertain exercise-induced brain changes.
FIGURE 6
FIGURE 6
The L-M1 to aDMN Z(CC)DIFF significantly predicts the amount of change in the Halstead test of Psychomotor speed (p = 0.01, cluster size = 50). The extracted ROI Z(CC)DIFF accounts for 57% of variance in the change in Halstead score after a 12-week intervention. Closed circles = AE; Open circles = BAL.
FIGURE 7
FIGURE 7
The difference in left and right M1 connectivity (L-RM1), as calculated with Equation 4 PRE and POST 12-week exercise intervention. The hot colors represent areas where the left M1 is more connected than the right M1, and the cool colors represent the opposite. The blank areas contain voxels where left and right M1 have similar or no connectivity. The percentage values in yellow denote the proportion of voxels within one hemisphere compared to total of both hemispheres within each session. Notice that from pre to post, the left hemisphere L-RM1 area expands (from 32 to 51%), whereas the right hemisphere L-RM1 area contracts (68–49%). Plotting the average connectivity strength in the voxels with changing area, R-M1 connectivity to the left hemisphere is reduced after 12-weeks of exercise intervention while the L-M1 connectivity is maintained or slightly increased. L-M1 connectivity increases and R-M1 connectivity decreases in the voxels with changing areas. After a 12-week exercise intervention (AE or BAL), the group average M1 connectivity profile is balanced across hemispheres. Δarea pink = pre area, Δarea green = post area.

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