Elsevier

NeuroImage

Volume 20, Issue 2, October 2003, Pages 1171-1180
NeuroImage

Regular article
Functional cerebral reorganization following motor sequence learning through mental practice with motor imagery

https://doi.org/10.1016/S1053-8119(03)00369-0Get rights and content

Abstract

The goal of the present study was to examine, via positron emission tomography, the functional changes associated with the learning of a sequence of foot movements through mental practice with motor imagery (MI). Following intensive MI training over several days, which led to a modest but significant improvement in performance, healthy subjects showed an increase in activity restricted to the medial aspect of the orbitofrontal cortex (OFC), and a decrease in the cerebellum. These main results are largely consistent with those found in a previous study of sequence learning performed in our laboratory after physical practice of the same task [NeuroImage 16 (2002) 142]. Further analyses showed a positive correlation between the blood flow increase in the OFC and the percentage of improvement on the foot sequence task. Moreover, the increased involvement of the medial OFC revealed a modality specific anatomo-functional organization, as imagination of the sequential task after MI practice activated a more posterior region than its execution. These results demonstrate that learning a sequential motor task through motor imagery practice produces cerebral functional changes similar to those observed after physical practice of the same task. Moreover, the findings are in accord with the hypothesis that mental practice with MI, at least initially, improves performance by acting on the preparation and anticipation of movements rather than on execution per se.

Introduction

Motor imagery (MI) is defined as an active process during which the representation of a specific action is internally reproduced within working memory, without any corresponding motor output (Decety and Grèzes, 1999). An increasing number of investigations have recently studied the neurophysiological correlates of this process and have aimed at clarifying the relationship between executed and imagined movements. Part of this effort stems from a need to explain the underlying mechanisms by which mental practice (MP) with MI improves the learning of motor skills (Jackson et al., 2001). Indeed, results from sport psychology and skill-learning studies show that MP with MI improves subjects' performance when compared to no-practice control conditions, albeit to a lesser extent than physical practice alone Feltz and Landers, 1983, Driskell et al., 1994. These findings suggest that MP with MI can be effective at improving the learning of motor skills. However, the neural substrate mediating the beneficial effects of MI training remains unknown.

In one of the rare brain mapping studies designed to examine the effect of MI practice on motor learning, Pascual-Leone and colleagues (1995) showed, through transcranial magnetic stimulation, that representational maps in the contralateral primary motor cortex for long finger flexor and extensor muscles expand after learning a one-handed piano exercise with either physical or MI practice. Such a finding suggests that mental training with MI produces representational cortical changes comparable to those elicited through physical practice. Thus, based on these results and the growing body of evidence showing a neurophysiological similarity between executed and imagined movements, we have recently proposed that changes in performance on motor skill learning tasks following mental practice using motor imagery would be associated with a functional cerebral reorganization similar to that reported after physical practice (Jackson et al., 2001).

As a first step to test this hypothesis, Lafleur and colleagues (2002) measured, through positron emission tomography (PET), the dynamic changes in cerebral activity before and after physical practice of an explicitly known sequence of foot movements. Changes in regional cerebral blood flow (rCBF) associated with physical execution of the sequence early in the learning process were observed bilaterally in the dorsal premotor cortex and cerebellum, as well as in the left inferior parietal lobule. After training, however, most of these brain regions were no longer significantly activated, suggesting that they were critical for establishing the cognitive strategies and motor routines involved in executing sequential foot movements. In contrast, after practice, an increased level of activity was seen bilaterally in the medial orbitofrontal cortex and striatum, as well as in the left rostral–ventral portion of the anterior cingulate cortex and a different region of the inferior parietal lobule, suggesting that these structures play an important role in subsequent stages of motor learning. Finally, and most importantly, a similar pattern of dynamic changes was observed during acquisition of a motor sequence through physical practice whether the movements were executed or imagined, suggesting that both modalities can reflect the cerebral plasticity occurring during the learning of this skilled behavior.

In the present study, we sought to measure cerebral functional changes associated with the learning of the same sequential motor skill, but this time after intensive training using MI practice instead of physical practice. It was predicted that MP with MI, like physical practice, would lead to cerebral reorganization in a network of structures that involves both the cortico–striato–thalamo–cortical and cortico–cerebello–thalamo–cortical loops (see Penhune and Doyon, 2002, Doyon et al., 2003. More specifically, we expected learning-related increases in rCBF in the anterior cingulate cortex, striatum, medial orbitofrontal region, and inferior parietal lobule. We also expected a significant decrease of activity in the cerebellum after practice.

Section snippets

Subjects

Nine right-handed and right-footed healthy subjects (five women, four men; mean age = 26 years, SD = 3.9) took part in this study. The protocol was approved by the Ethics Committee of the Montreal Neurological Institute, and all subjects gave informed written consent before participating.

Foot sequence task

The apparatus consisted of a pedal that allowed free upward (dorsiflexion) and downward (plantarflexion) single-joint movements of the left ankle (see Lafleur et al., 2002, for a more detailed description of

Behavioral measures

Fig. 2a shows the average response time in milliseconds for all subjects in the Random Execution and the Sequence Execution conditions both before (Early Learning) and after mental practice (Late Learning). Descriptive statistics show the group's average performance in the Sequence condition improved from 486 ± 61 ms to 436 ± 54 ms and that seven out of nine subjects decreased their average response time after practice (not shown). Using a critical alpha level set at 0.05, a 2 × 2 (Condition ×

Discussion

The behavioral results of the present study confirmed that MP with MI of a novel foot-sequence task can improve motor performance. Indeed, the observed reduction in response time, which was specific to the practiced sequence, strongly suggests that learning of the sequence of foot movements occurred in addition to a nonspecific improvement to use the apparatus (i.e., random condition). Moreover, the parallel and significant decrease in the time taken to imagine the sequence also implies

Conclusion

Our results provide the first evidence that learning of a motor sequence through MP with MI elicits, initially, functional changes in the corticocerebellar system, as well as within the medial orbitofrontal cortex. These findings, together with the absence of any change of activity in the striatum and the premotor cortex following extended mental practice, suggest that this form of training acts more on the nonconscious preparation/anticipation of movements involved in a motor sequence, than on

Acknowledgements

We thank the subjects who participated in this study. We also thank Kate Hanratty and Isabelle Deaudelin for their technical assistance. We would also like to acknowledge the anonymous reviewer for the constructive criticism made to an earlier version of this manuscript. This work was supported by a grant from the National Center for Excellence to J.D., F.M., and C.R., a grant from the National Science and Engineering Research Counsel to J.D., and a scholarship from the FRSQ/REPAR to P.J.

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