Elsevier

Behavioural Brain Research

Volume 223, Issue 2, 1 October 2011, Pages 280-286
Behavioural Brain Research

Research report
Non-effective increase of fMRI-activation for motor performance in elder individuals

https://doi.org/10.1016/j.bbr.2011.04.040Get rights and content

Abstract

Motor performance declines with increasing age and it has been proposed that elder people might compensate for these deficits with increased cerebral activation. However, it is not known, whether increased activation – especially in motor areas of the contralateral and the ipsilateral cerebral hemisphere – might effectively contribute to motor performance or whether it is an ineffective way to counteract age related deficits in the motor system. We tested this question by mapping brain activation during performance of differentially demanding motor tasks in 18 young (mean 25.39 years) and 17 elderly (mean 66.65 years) healthy individuals. We tested a wide range of hand motor tasks from passive wrist movements, fist clenching at different frequencies, to a somatosensory-guided finger pinch task. In the elderly group functional activation was generally increased for all tasks with comparable motor performance for ipsilateral primary and secondary motor areas. The young group showed increased contralateral primary motor cortex activation for the more difficult somatosensory guided precision grip task. We correlated motor performance of the task with high difficulty and comparable performance with fMRI-activation. Elder participants showed a negative correlation for the ipsilateral supplementary motor area (SMA) and for the ipsilateral sensorimotor cortex (SM1). Young participants showed a positive correlation for contralateral SMA and SM1. Our data suggest an increased cerebral recruitment reflects an inefficient response to an age-related higher difficulty of task and is not an effective way to counteract age-related deficits in the motor system.

Highlights

► Elder subjects showed increased activation during performance of different motor tasks. ► Functional increase in ipsilateral motor areas were characteristic for the elderly. ► Functional increase in contralateral motor areas was specific for the younger. ► Functional increase in the elderly represents an ineffective attempt for compensation.

Introduction

Motor performance decreases linearly in individuals older than 60 years for less demanding tasks and nonlinearly for complex movements [20]. The decline in motor performance with increasing age is associated with a structural decline in the neuromuscular system [4], [10] and central neuronal changes [14]. For other domains, it has been demonstrated that cortical representation in elderly people, as investigated with functional magnetic resonance imaging (fMRI), differs from that in younger persons, even when the level of performance is matched [1]. Generally, task-related activation appears to be more focused and lateralized in younger individuals and more diffuse and bilateral in older individuals [1], [26]. For the motor domain the reduction of functional lateralization, especially as a result of ipsilateral activation, correlates with age [16].

For the elderly functional mapping studies on simple motor tasks revealed increased activation in contralateral primary and secondary motor regions (M1, dPMC, SMA [9], [14] and parietal cortex [9], [14], but also in ipsilateral M1 [15], [16], [18], [28], dPMC [15], [18], and SMA [2], [15].

These studies with younger and older individuals were based on experiments testing activation differences during the performance of simple motor tasks. However, highly demanding motor tasks are the first to show a decline in aged individuals [20] and should therefore be more distinguishable between groups. As an example of a more challenging motor paradigm, Heuninckx et al. [8] used an interlimb coordination task and found a positive correlation between performance and BOLD-signal of areas additionally activated by the elderly. The authors conclude that age-related changes are compensational and increased activation in the older participants is associated with better performance. This effective compensation hypothesis emphasizes that increased activation, especially in non-motor-areas, is associated with increased performance, and is therefore able to compensate for motor deficits. In older individuals, additionally activated areas – especially non-motor regions – should correlate positively with performance. However, in this study, the performance level between groups differed and is therefore only comparable in certain aspects. In contrast, a compensation of decreased motor ability should be successful in simple, repetitive motor tasks. It might be insufficient in those tasks that show a high demand with respect to sensory guidance or to movement complexity or velocity.

Consequently, we investigated differently demanding motor tasks (repetitive simple active and passive movements, more difficult somatosensory guided movements) in the same group of healthy volunteers and we compared representation maps of young and old individuals involved in different levels of motor performance. In order to differentiate the functional relevance of representation sites we correlated motor representation during tasks with performance. We assumed that this approach might answer the question whether increasing activation in a highly demanding motor task is capable to effectively compensate for age related decline in motor function.

Section snippets

Participants

Overall, 35 volunteers participated in this study including 18 younger individuals (7 males, 11 females, age range 23–30 years, average age 25.39 years) and 17 elderly individuals (2 males, 15 females, age range 57–72, average age 66.65 years). All participants were right-handed [average score of handedness: 90.86 ± 12.02 [17] and performed all tasks with their dominant hand. All participants were healthy, without any neural or cardio-vascular disease and were not taking any regular medication.

Motor performance

Older participants matched the performance level of the younger ones for all motor conditions (see Table 1).

fMRI findings; main effects

A detailed listing of activation sites during each task is provided in the Supplementary Table 1. In the group of young participants passive wrist movements evoked cortical activation in MCC, contralateral SMA, dPMC and bilateral SM1, S2, BA 5, BA 7 and BA 44, as well as cerebellar activation was higher ipsilateral to movement execution.

During the fist-clenching task at 1 Hz, young

Discussion

By using a combined approach of mapping movements with different motor demand in younger and older individuals together with correlation analysis of performance with fMRI-activation, we demonstrated that an activation increase in the elderly was not associated with effective performance compensation. Accordingly, we observed increased activation in ipsilateral motor areas in the elderly during all types of movement and we found a negative correlation of fMRI-activation in the ipsilateral SMA

Acknowledgements

This study has been supported by a starting grant of the University of Greifswald and by the DFG (LO 795/7-1).

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