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Accordingly, our results provided strong support for the compensation hypothesis. Interestingly, this positive association between performance and brain activity was not evident across the entire brain but rather in some specific, well defined regions that were either recruited by both age groups or additionally recruited by the elderly compared with the young group. These regions were activated by both age groups and represent typical motor regions that are usually activated by ipsilateral hand—foot movements Ehrsson et al.
Especially SMA and cerebellar activity are hypothesized to reflect increasing demands on motor timing Ivry, ; Macar et al. Therefore, the observed positive correlations between coordination performance and brain activity in these motor regions may reflect a successful compensatory response to increased functional demands by the high-performing elderly. Interestingly, besides typical motor regions, more remote regions were also additionally recruited in the elderly and correlated positively with performance on the coordination task. First, positive correlations were observed in the contralateral superior parietal cortex, contralateral posterior cerebellum, and ipsilateral anterior cerebellum, which were previously shown to be involved in higher-order sensorimotor coordination during more demanding tasks Debaere et al.
Whereas the cerebellum is a typical timing and coordination organ see above , the superior parietal cortex is strongly involved in sensorimotor integration and spatial aspects of movement planning Wenderoth et al. Both spatial and temporal integration are critical features of successful interlimb coordination.
Second, we also identified several nonmotor regions that were additionally recruited by the elderly as well as related to successful motor performance. The IFGPO, anterior insula and superior temporal gyrus appear to be involved in higher-order auditory processing Platel et al.
This suggests that older subjects made more pervasive use of external information sources for controlling their limb movements by means of the metronome-pacing signal, which resulted in more accurate coordination performance. Furthermore, the IFGPO and IFGPT are involved in interfacing external information about biological motion with internal representations of limb actions, as observed during movement observation, imitation, or imagery Grezes et al. Together, the higher activations of these regions appear to reflect higher-level processing and integration of external and internal information sources to successfully guide motor coordination.
Finally, positive correlations between level of coordination performance and activation were observed in two regions in the contralateral frontal lobe i. There is increasing agreement that the pre-PMd is more closely related to cognitive than to motor processes.
The DLPFC receives visual, somatosensory, and auditory information from the occipital, temporal, and parietal cortices Goldman-Rakic and Schwartz, ; Barbas and Pandya, ; Seltzer and Pandya, ; Pandya and Yeterian, ; Petrides and Pandya, and has preferential connections with the motor system structures Miller and Cohen, Overall, the observed positive correlations between coordination accuracy and activation in the pre-PMd and DLPFC suggest that the older subjects relied on increased cognitive monitoring that had a beneficial impact on complex coordination performance, suggesting that the additional neural recruitment was compensatory.
Similarly, when groups of good versus bad performing elderly were compared, good performers exhibited more brain activation than bad performers Cabeza et al. In the present motor coordination study, the compensatory recruitment extended far beyond the prefrontal regions and involved a more extensive network, suggesting that such tasks are very instrumental to studying age-related alterations in complex brain function.
Coordination in the elderly was associated with profound activations in 1 classical motor control regions, 2 higher-level sensorimotor regions reflecting increased reliance on sensory information processing, and 3 frontal regions reflecting increased cognitive control and performance monitoring. Importantly, the majority of these regions exhibited a positive correlation between brain activation level and performance in the elderly, such that increased recruitment in these regions was associated with higher motor coordination accuracy.
This enabled some elderly to reach motor performance levels comparable to those obtained in the younger controls, suggesting that the additional recruitment is meaningful for preserving motor performance in the elderly i.
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However, compensatory recruitment might have a hidden cost. Reuter-Lorenz and K. Cappell, unpublished observation. This may perhaps explain why poorly performing older adults showed BOLD responses similar to those of the young participants, whereas the successful elderly exhibited more elaborate activation than young adults in some brain regions. In contrast to recent cognitive aging studies in which compensatory recruitment was established in the prefrontal regions, the present study showed activation across a more elaborate network that was dedicated to increasing cognitive control and enhanced processing of sensory information for motor performance, indicative of systems-level neuroplasticity at higher age.
Recent Activity. The snippet could not be located in the article text. This may be because the snippet appears in a figure legend, contains special characters or spans different sections of the article. J Neurosci. PMID: Stephan P. Leuven, B Heverlee, Belgium. Corresponding author. Correspondence should be addressed to Dr. Leuven, Tervuursevest , B Heverlee, Belgium. This article has been cited by other articles in PMC. Abstract Functional imaging studies have shown that seniors exhibit more elaborate brain activation than younger controls while performing motor tasks.
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Keywords: aging, fMRI, motor control, interlimb coordination, cognition, compensation, dedifferentiation, neuroplasticity. Introduction One of the most prominent challenges of current society is to develop a better understanding of the aging process. Materials and Methods Participants Twelve young adults mean age, Open in a separate window.
Neuro-Behavioral Determinants of Interlimb Coordination : Stephan P. Swinnen :
Figure 1. Between-group conjunction: regions similarly activated in the young and the elderly. Between-group analysis: determining differentially activated regions. Within-group analyses: correlation between motor performance and brain activation with respect to similarly and differentially activated regions. Table 1. Kinematic results. Figure 2. Within-group analyses: correlation between motor performance and brain activation with respect to the similarly activated regions In this section, areas are reported that exhibit a significant correlation with performance and are similarly activated in both age groups.
Table 2. No region was significantly more activated in the younger than older group.
Figure 3. Within-group analyses: correlations between motor performance and brain activation with respect to differentially activated regions In this section, areas are reported that exhibit a significant correlation with performance and are significantly overactivated in the elderly.
Table 3. Discussion The aim of the present study was to investigate whether age-related overactivation during motor performance reflects compensation or dedifferentiation mechanisms. Overactivated regions in the elderly, exhibiting a positive association between brain activity level and motor performance Interestingly, besides typical motor regions, more remote regions were also additionally recruited in the elderly and correlated positively with performance on the coordination task. Summary and conclusions Coordination in the elderly was associated with profound activations in 1 classical motor control regions, 2 higher-level sensorimotor regions reflecting increased reliance on sensory information processing, and 3 frontal regions reflecting increased cognitive control and performance monitoring.
Footnotes This work was supported by a grant from the Research Council of K. Preferential coupling between voluntary movements of ipsilateral limbs. Neurosci Lett. Differential control of in-phase and anti-phase coupling of rhythmic movements of ipsilateral hand and foot.
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J Mot Behav. Brain areas involved in interlimb coordination: a distributed network. Cerebellar and premotor function in bimanual coordination: parametric neural responses to spatiotemporal complexity and cycling frequency. General and task-specific frontal lobe recruitment in older adults during executive processes: a fMRI investigation of task-switching. Simultaneous movements of upper and lower limbs are coordinated by motor representations that are shared by both limbs: a PET study. Eur J Neurosci.
J Psychiatr Res. Analysis of fMRI time-series revisited. Statistical parametric maps in functional imaging: a general linear approach. Functional neuroanatomy of the primate isocortical motor system. Anat Embryol Berl ; — Interdigitation of contralateral and ipsilateral columnar projections to frontal association cortex in primates. Introduction to the special section on aging, cognition, and neuroimaging.
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Evidence from functional neuroimaging of a compensatory prefrontal network in Alzheimer's disease. Top-down effect of strategy on the perception of human biological motion: a PET investigation.