Neural basis of aging: the penetration of cognition into action control

Abstract

Although functional imaging studies have frequently examined age-related changes in neural recruitment during cognitive tasks, much less is known about such changes during motor performance. In the present study, we used functional magnetic resonance imaging to investigate age-related changes in cyclical hand and/or foot movements across different degrees of complexity. Right-handed volunteers (11 young, 10 old) were scanned while performing isolated flexion-extension movements of the right wrist and foot as well as their coordination, according to the "easy" isodirectional and "difficult" nonisodirectional mode. Findings revealed activation of a typical motor network in both age groups, but several additional brain areas were involved in the elderly. Regardless of the performed motor task, the elderly exhibited additional activation in areas involved in sensory processing and integration, such as contralateral anterior insula, frontal operculum, superior temporal gyrus, supramarginal gyrus, secondary somatosensory area, and ipsilateral precuneus. Age-related activation differences during coordination of both segments were additionally observed in areas reflecting increased cognitive monitoring of motor performance, such as the pre-supplementary motor area, pre-dorsal premotor area, rostral cingulate, and prefrontal cortex. In the most complex coordination task, the elderly exhibited additional activation in anterior rostral cingulate and dorsolateral prefrontal cortex, known to be involved in suppression of prepotent response tendencies and inhibitory cognitive control. Overall, these findings are indicative of an age-related shift along the continuum from automatic to more controlled processing of movement. This increased cognitive monitoring of movement refers to enhanced attentional deployment, more pronounced processing of sensory information, and intersensory integration.

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 segments are moved in opposite directions).

Figure 2.

Group mean activations for each motor task (A, HAND; B, FOOT; C, ISODIR coordination; D, NONISODIR coordination) versus REST overlaid on standard MNI renders and templates. Significant voxels (p < 0.001; corrected for multiple comparisons) are indicated in blue for the old group, in yellow for the young group, and in green for overlap between activation of both groups; in each, the height threshold is t = 6.98. L, Left hemisphere; R, right hemisphere.

Figure 3.

A-F, Statistical parametric mappings representing significantly larger activation in the old compared with the young group during isolated HAND and FOOT movements, resulting from the following conjunction analysis: [(Hand-Rest)_old vs (Hand-Rest)_young] ∩ [(Foot-Rest)_old vs (Foot-Rest)_young]. Significant voxels (p < 0.05; corrected for multiple comparisons) are indicated in the red spectrum, and the height threshold is t = 3.60. L, Left hemisphere; R, right hemisphere; FG, fusiform gyri; SMG, supramarginal gyrus; STG, superior temporal gyrus.

Figure 4.

A-L, Statistical parametric mappings representing significantly larger activation in the old group compared with the young group during ISODIR and NONISODIR coordination, resulting from the following conjunction analysis: [(ISODIR-Rest)_old vs (ISODIR-Rest)_young] ∩ [(NONISODIR-Rest)_old vs (NONISODIR-Rest)_young]. Significant voxels (p < 0.05; corrected for multiple comparisons) are indicated in the red spectrum, and the height threshold is t = 3.60. L, Left hemisphere; R, right hemisphere; sup. temporal gyrus, superior temporal gyrus. Bar plots show the estimated BOLD responses in arbitrary units for the different movement conditions and for both groups: a, old hand; b, old foot; c, old ISODIR; d, old NONISODIR; e, young hand; f, young foot; g, young ISODIR; h, young NONISODIR.

Figure 5.

A-H, Statistical parametric mappings representing significantly larger activation in the old group compared with the young group with respect to the comparison of nonisodir versus isodir hand-foot coordination. significant voxels (p < 0.05; corrected for multiple comparisons) are indicated in the red spectrum, and the height threshold is t = 3.60. l, left hemisphere; r, right hemisphere; og, occipital gyrus; ppc, posterior parietal cortex; ant. cerebellum, anterior cerebellum; post. cerebellum, posterior cerebellum.