Elsevier

Clinical Neurophysiology

Volume 122, Issue 1, January 2011, Pages 153-162
Clinical Neurophysiology

Plasticity of motor cortex induced by coordination and training

https://doi.org/10.1016/j.clinph.2010.05.022Get rights and content

Abstract

Objective

To study the modifications induced by training of a coordinated movement on the primary motor cortex (M1) maps of one proximal muscle and one distal muscle activated alone and during their co-contraction.

Methods

Six healthy female sport students performed a 6-week training program during which they were trained in darts 3–4 times a week. At the end each subject had made more than 1200 throws. Transcranial magnetic stimulation (TMS) was used to map the proximal medial deltoid (MD) and the distal brachio-radialis (BR) muscle representations on M1. Motor evoked potentials (MEPs) amplitude and excitability curves were used to test corticomotor excitability.

Results

The cortical representation areas of each muscle separately increased after training. The cortical representation and the excitability curve of the BR muscle increased during co-activation with the MD. Combining co-contraction and training produced a further enlargement of the M1 representation of the BR muscle.

Conclusions

The enlargement of the BR representation in M1 suggests the development of overlapping zones specifying functional synergies between distal and proximal muscles.

Significance

Our findings support the idea that training of a coordinated movement involving several muscles and joints requires an activity-dependent coupling of cortical networks.

Introduction

In healthy humans, the ability to learn novel motor skills through practice is accompanied by functional reorganization of the motor system including the primary motor cortex (M1) (Pascual-Leone et al., 1994, Karni et al., 1995, Nudo et al., 1996, Classen et al., 1998). Motor practice induces changes in cortical motor representation that can be measured with transcranial magnetic stimulation (TMS). The changes are principally an enlargement of the cortical representation of the muscle used in the task and a facilitation of the motor evoked potentials (MEPs), indicating an increase in cortical excitability. In short-term motor learning studies, cortical changes can be observed for a few minutes (Garry et al., 2004), whereas learning a piano sequence produces more pronounced changes (Pascual-Leone et al., 1994, Pascual-Leone et al., 1995). Classen et al. (1998) used TMS to evoke isolated and directional thumb movements and showed that training modified the thumb cortical networks, which encoded movement kinetics. This suggests a short-term memory for movement that is the first step in skill acquisition (Classen et al., 1998, Karni et al., 1995). Most of the cited studies were focused on distal hand muscles known to have larger cortical representations and explored the effects of short-term plasticity on their cortical representations.

TMS has been used to map cortical representations of different muscles at rest (Wassermann et al., 1992) and during low level activity (Wilson et al., 1995). Motor cortex representations in humans have shown discrete amplitude peaks included within a diffuse representation. Maps of different upper extremity muscles overlapped on the motor cortex in spite of a lateral shift (Penfield and Rasmussen, 1950). The threshold for the activation of proximal muscles by transcranial electrical stimulation (TES, Rothwell et al., 1987) or TMS (Wassermann et al., 1992) was higher than for distal muscles. A low level voluntary contraction permitted the observation of MEPs at a lower rate of stimulation (Wilson et al., 1995), especially for proximal muscles of the upper extremities that were difficult to map at rest (Levy et al., 1991; see Amassian et al., 1995). Since Penfield and Boldrey, 1937, Penfield and Rasmussen, 1950, the large representation of distal muscles has been generally associated with a fine level of control. Cortical maps revealed some size differences depending on handedness and the muscle location (proximal versus distal). Wassermann et al. (1992) showed that distal muscle representations were larger than proximal ones, and that they were larger for the dominant side, contrary to proximal muscles.

A few studies have investigated the changes of proximal muscle representation induced by motor practice (see Tyč and Boyadjian, 2006). Liepert et al. (1999) have shown that short-term training of synchronous thumb and foot movements modified motor output maps due to interactions between hand and foot representation areas in M1. This result indicated a shift of the thumb motor output map towards the leg map. Changes in hand muscle corticomotor excitability in relation to static shoulder positions have been interpreted as a proximal–distal synergism operating through reaching movements (Ginanneschi et al., 2005). More recently, comparison of the effects of short-term training at proximal and distal upper limb joints, revealed a greater effect on the pathways controlling the index finger and a smaller effect on pathways controlling more proximal joints (Krutky and Perreault, 2007). These findings suggested a difference in the motor cortical contributions to short-term motor plasticity in the pathways controlling proximal and distal joints in the upper limb. Ackerley et al. (2007) used TMS to explore whether training in different coordination patterns affects the development of motor plasticity. A simple repetitive thumb movement made in synchrony, or in syncopation, with respect to an auditory metronome, shifted both synchronized and syncopated motor practice modified thumb movements in the trained direction. These studies have raised questions about the role of the motor cortex in coordinating multi-joint movements and the impact of training. To date, it has not been established whether long-term training of a complex coordinated movement affects the cortical representation of muscles during their co-activation.

In a previous study, we examined the effect of highly-skilled behaviour on motor cortex representations of upper extremity muscles in volleyball players. We showed an expansion of proximal muscle representation in the contralateral M1 with an increase in overlap between proximal and distal muscle representations (Tyč et al., 2005). This overlap was suggested to play a role in muscle control during coordinated multi-joint movements. It was consistent with other findings that generated the hypothesis that M1 could control the different limb segments as a whole rather than individually (Scott, 2000). For example, shoulder, elbow and wrist muscle activation during pointing movements appeared to involve common motor cortical circuits (Devanne et al., 2002). As Schieber (2001) has suggested, an organization of the motor cortex with larger representations of the proximal muscles overlapping those of the distal muscles might facilitate coordination and motor learning.

The purpose of the present study was to use TMS to further analyze the changes in cortical representations of a shoulder muscle and of a forearm muscle used to execute a complex coordinated movement. The key parameters in our protocol were the learning of a coordinated complex movement, the co-contraction of a proximal and a distal muscle, and long-term motor training. We chose the traditional game of darts, in which all joints in an upper limb are involved in a specific coordination pattern and timing of proximal and distal muscles (Temprado et al., 1997). We report the changes in the cortical representations of the proximal medial deltoid (MD) and the distal brachio-radialis (BR) muscles following a six-week training period together with an enlargement of the scalp-evoked motor maps when the two muscles are co-contracted.

Part of this work has been presented in abstract form (Tyč and Boyadjian, 2008).

Section snippets

Subjects

Studies conforming to the standards set by the declaration of Helsinki were carried out on six healthy female sport students (mean age 21 ± 0.26) who did not regularly participate in a sport involving specific arm activity. All subjects gave their free informed written consent for the study. All subjects were right-handed according to the Edinburgh Handedness Inventory (Oldfield, 1971).

Training protocol

The subjects participated in a six-week training program during which they trained at throwing darts 3–4 times a

Results

The six-week training period induced an increase in the performance in the throwing test for each subject. Before training, the 15 throws test resulted in a score between 47 and 89 points with a mean of 70 points for the six subjects (4.7 points per dart). The score after training was 77 to 112 points with a mean of 94 points (6.3 points per dart).

The aMT were stable and no statistical difference was observed throughout the training session for each subject and for both muscles. The aMT of the

Discussion

The principal finding of the present study is that co-activation of the proximal MD muscle with the distal BR muscle enlarges the cortical representation of the BR muscle and that a six-weeks training period produces an enlargement of the cortical motor representations of the co-contracted muscle.

Acknowledgements

We thank our students for giving their time to participate in this study. We thank Professor A.R. Lieberman for editing our manuscript and correcting the English language. We are grateful to Professor John C. Rothwell for his advice.

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