Systems neuroplasticity in the aging brain: recruiting additional neural resources for successful motor performance in elderly persons

Abstract

Functional imaging studies have shown that seniors exhibit more elaborate brain activation than younger controls while performing motor tasks. Here, we investigated whether this age-related overactivation reflects compensation or dedifferentiation mechanisms. "Compensation" refers to additional activation that counteracts age-related decline of brain function and supports successful performance, whereas "dedifferentiation" reflects age-related difficulties in recruiting specialized neural mechanisms and is not relevant to task performance. To test these predictions, performance on a complex interlimb coordination task was correlated with brain activation. Findings revealed that coordination resulted in activation of classical motor coordination regions, but also higher-level sensorimotor regions, and frontal regions in the elderly. Interestingly, a positive correlation between activation level in these latter regions and motor performance was observed in the elderly. This performance enhancing additional recruitment is consistent with the compensation hypothesis and characterizes neuroplasticity at the systems level in the aging brain.

Figures

Figure 1.

Cyclical ipsilateral coordination of the hand and foot according to the isodirectional mode (A; both limb segments are moved in the same direction) and the nonisodirectional mode (B; both limb segments are moved in opposite directions).

Figure 2.

Statistical parametric maps representing brain regions that were similarly activated by both age groups, resulting from the following conjunction analysis: (NONISODIR − rest)old∩ (NONISODIR − rest)young. Significant voxels (p < 0.05; corrected for multiple comparisons) are indicated in the red spectrum, and the height threshold is t = 4.00. L, Left hemisphere; R, right hemisphere. White arrows indicate brain regions that exhibit a significant correlation between brain activity level and coordination performance, as identified by a whole-brain multiple regression analysis followed by a small-volume correction with the similarly activated clusters as shown in the statistical parametric maps (p < 0.05, FDR corrected within the search volume; for details, see Materials and Methods). The graphics display each subject's BOLD response with respect to the within-cluster peak activation as a function of the inverse of phase error (1/AE), with the younger subjects in blue and the older subjects in red.

Figure 3.

Statistical parametric maps representing significantly larger activation in the old compared with the young group during the NONISODIR coordination mode, resulting from the following contrast: (NONISODIR − rest)old versus (NONISODIR − rest)young. Significant voxels (p < 0.05; corrected for multiple comparisons) are indicated in the red spectrum, and the height threshold is t = 4.00. L, Left hemisphere; R, right hemisphere. White arrows indicate brain regions that exhibit a significant correlation between brain activity level and coordination performance, as identified by a whole-brain multiple regression analysis followed by a small-volume correction with the clusters, overactivated by the elderly as shown in the statistical parametric maps (p < 0.05, FDR corrected within the search volume; for details, see Materials and Methods). The graphics display each subject's BOLD response with respect to the within-cluster peak activation as a function of the inverse of the phase error (1/AE), with the younger subjects in blue and the older subjects in red.