Elsevier

Cortex

Volume 44, Issue 9, October 2008, Pages 1271-1278
Cortex

Note
Decline in motor prediction in elderly subjects: Right versus left arm differences in mentally simulated motor actions

https://doi.org/10.1016/j.cortex.2007.07.008Get rights and content

Abstract

This study investigates the effects of age upon the temporal features of executed and imagined movements performed with the dominant (D; right) and nondominant (ND; left) arms. Thirty right-handed subjects were divided into two groups: (i) the young group (n = 15; mean age: 22.5 ± 2.5 years) and (ii) the elderly group (n = 15; mean age: 70.2 ± 2.2 years). The motor task, involving arm pointing movements among four pairs of targets (.5 cm, 1 cm, 1.5 cm and 2 cm), imposed strong spatiotemporal constraints. During overt performance, young and elderly subjects modulated movement duration according to the size of targets, despite the fact that movement speed decreased with age as well as in the left arm compared with the right. This observation was also valid for the covert performance produced by the young group. However, such a strong relationship between covert movement durations and target size was not as obvious in the elderly group. Young, compared to elderly subjects, showed stronger correlations and smaller absolute differences between executed and imagined movements for both arms. Additionally, the absolute difference between executed and imagined arm movement durations was more pronounced for the left than the right arm in aged subjects. This result suggests a selective decline with age of mental prediction of motor actions, which is more prominent when the ND arm is involved.

Introduction

Motor imagery, a concept similar to internal movement simulation or covert movement execution, is a state of mental rehearsal during which a subject replicates a motor action without moving the limbs or activating the muscles involved in the execution of the same action. Internal simulation of single movements or movement patterns has been shown to recruit neural networks overlapping with those activated during overt movement performance. For instance, exploration of brain activity during overt or covert movements revealed a common activation of the parietal and prefrontal cortices, the supplementary motor area, the premotor and primary motor cortices, the basal ganglia and the cerebellum (Decety, 1996, Fadiga and Craighero, 2004, Jeannerod, 2001). At the behavioural level, using the mental chronometry paradigm in various motor tasks (arm pointing, writing, and walking), several studies have shown that covert actions preserve the same spatiotemporal characteristics and obey the same motor rules or biomechanical constraints as their overt counterparts (Courtine et al., 2004, Decety et al., 1989, Gentili et al., 2004, Maruff et al., 1999, Papaxanthis et al., 2002a, Papaxanthis et al., 2002b, Papaxanthis et al., 2003). These neurocognitive similarities between sensorimotor and mental states highly support the simulation theory developed by Jeannerod (2001). This theory postulates that covert actions are part of motor representations and are related to the higher levels of the central nervous system involved in motor planning and prediction.

However, while the simulation theory is corroborated by several results in young individuals, little information is available regarding its validity in normal/healthy aging. This question is relevant because clear differences emerge when performance and brain activation are compared between elderly and young people during cognitive or motor tasks. For example, in memory-related tasks (i.e., episodic memory, spatial working memory, etc.), in which old people perform less well than young people do, task-specific underactivation of localised brain regions is detected in elderly subjects. Intriguingly, when elderly and young people perform equally, an important bilateral activation emerges in elderly people. Thereby, aged subjects engage more brain regions during task execution (Logan et al., 2002, Reuter-Lorenz, 2002, Mattay et al., 2002, Ward and Frackowiak, 2003). Similar investigations, examining motor performance in relatively simple motor tasks, have shown that elderly subjects recruit additional cortical and subcortical areas (Heuninckx et al., 2005).

Age-related modifications in corticospinal control of upper limb muscles have been observed in transcranial magnetic stimulation experiments. Precisely, these investigations have indicated a decline in the amplitude of motor evoked potentials (MEPs) during simple isometric contractions and a reduction in cortical inhibitory mechanisms in aged people (Sale and Semmler, 2005). Since normal aging strongly influences cognitive functions (Briggs et al., 1999, Dror and Kosslyn, 1994, Logan et al., 2002, Raz et al., 1999, Reuter-Lorenz, 2002) and sensorimotor control of movement (Ketcham et al., 2002, Seidler-Dobrin and Stelmach, 1998, Seidler et al., 2002, Smith et al., 1999), one could expect mental operations related to motor prediction to be altered in elderly individuals. Hence, the general objective of the present study was to delineate internal simulation of motor actions as a function of normal aging. In particular, we investigated the effect of age upon temporal characteristics of covert and overt movements involving strong spatiotemporal constraints. In view of the fact that mental and motor processes become slower with age (Salthouse, 2000, Skoura et al., 2005) we anticipated a general decline of motor prediction in aged subjects. Furthermore, we examined if any deterioration in motor imagery with age could be related to the side of the limb involved in mental operations, i.e., the dominant (D; right) or the nondominant (ND; left) arm. It is not currently well-known if motor control, imagery and prediction are influenced by a lifetime of preferential use of the hand for skilled (D) and unskilled (ND) motor tasks. Such a question is pertinent as neural adaptations in corticospinal control of the left (ND) arm occur with age. For instance, Sale and Semmler (2005) found lower MEPs and shorter silent-period durations in the left hand of elderly compared with young subjects, whereas there was no age difference in the right hand. In addition, there are significant age-related differences in brain neural activity associated with repetitive movements of the hand, which were more prominent when using the ND hand (Hutchinson et al., 2002). Regarding these findings, we expected a stronger alteration in motor action covert stages when the left (ND) arm is recruited in elderly people.

Section snippets

Participants

Thirty volunteers (informed consent was signed), all right-handed, participated in the present study. Handedness was determined by means of the Edinburgh Handedness inventory (Olfield, 1971). Subjects also performed multiple behavioural tasks (writing, catching, grasping and throwing), which confirmed right arm dominance. Subjects were divided into two different groups as a function of age: (i) the young group (eight males and seven females; mean age: 22.5 ± 2.5 years), (ii) the elderly group

Movement precision and temporal variability

Young and elderly adults respected our requirements concerning spatial precision since few overt trials were repeated (respectively, 27 and 33 trials for the young and elderly groups). In addition, considering the total number of overt pointing movements between the targets (n = 24,000; 30 subjects × 4 target sizes × 2 arms × 10 trials × 10 movements within each trial), an insignificant number of targets were missed. The young group missed the targets 184 times (1.53%) and the elderly group missed them

Discussion

The present study was devoted to the exploration of the temporal features of executed and imagined arm movements in young and elderly adults. By using arm movements requiring high spatiotemporal constraints, we found significant differences in imagery ability between elderly and young subjects. Notably, for both the D and the ND arm, young adults showed stronger correlations and smaller absolute differences between executed and imagined movements than elderly subjects did. Furthermore, we

Acknowledgements

This work was supported by the Conseil Regional de Bourgogne, the INSERM and the CNRS.

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