La Plasticidad de La Corteza Motora Es Inducida Mediante Coordinacion y Entrenamiento 2011

8/22/2019 La Plasticidad de La Corteza Motora Es Inducida Mediante Coordinacion y Entrenamiento 2011

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Plasticity of motor cortex induced by coordination and training

F. Tyc*, A. Boyadjian

Laboratoire Plasticit et Physio-Pathologie de la Motricit, UMR 6196, CNRS, 31 Chemin J. Aiguier, 13402 Marseille Cedex 20, France

a r t i c l e i n f o

Article history:

Accepted 24 May 2010

Available online 17 June 2010

Keywords:

TMS

Motor cortex

Training

Coordination

Plasticity

Mapping

a b s t r a c t

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 34 times a week. At the end each subject had made more than 1200 throws. Trans-

cranial 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.

2010 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights

reserved.

1. Introduction

In healthy humans, theabilityto learn novel motor skillsthrough

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 practiceinduces changes in cortical motorrepresenta-

tion 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 corti-

cal 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, 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 hu-

mans have shown discrete amplitude peaks included within a dif-

fuse 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 observa-

tion 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) and Penfield (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 Tyc and Boyadjian,

1388-2457/$36.00 2010 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved.doi:10.1016/j.clinph.2010.05.022

* Corresponding author. Tel./fax: +33 3 20 74 85 66.

E-mail address: [email protected] (F. Tyc).

Clinical Neurophysiology 122 (2011) 153162

Contents lists available at ScienceDirect

Clinical Neurophysiology

j o u r n a l h o m e p a g e : w w w . e l s e v i e r . c o m / l o c a t e / c l i n p h
http://dx.doi.org/10.1016/j.clinph.2010.05.022mailto:[email protected]://dx.doi.org/10.1016/j.clinph.2010.05.022http://www.sciencedirect.com/science/journal/13882457http://www.elsevier.com/locate/clinphhttp://www.elsevier.com/locate/clinphhttp://www.sciencedirect.com/science/journal/13882457http://dx.doi.org/10.1016/j.clinph.2010.05.022mailto:[email protected]://dx.doi.org/10.1016/j.clinph.2010.05.022


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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 inter-

preted as a proximaldistal synergism operating through reaching

movements (Ginanneschi et al., 2005). More recently, comparisonof 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 sug-

gested 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 direc-

tion. These studies have raised questions about the role of the mo-

tor 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 (Tyc

et al., 2005). This overlap was suggested to play a role in muscle

control during coordinated multi-joint movements. It was consis-

tent 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 lar-

ger 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 ana-

lyze 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 prox-

imal 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) musclesfollowing 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 (Tyc and

Boyadjian, 2008).

2. Methods

2.1. 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 sportinvolving 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).

2.2. Training protocol

The subjects participated in a six-week training program during

which they trained at throwing darts 34 times a week. Each sub-

ject received a complete dart game set including a dartboard andthree darts. The dartboard was used on the side showing 10 con-

centric circles worth one point for the external circle and 10 points

for the centre. The throwing distance was indicated by a black line

on the floor set at 2.4 m from the dartboard. The subject had her

right hip facing the target, with her right foot on the black line

and threw the dart with her right arm. In this specific position

MD and BR muscles are co-contracted as shown by EMG recordings

(Fig. 1). During each training session the subject had to maintain

the same position at the same distance from the dartboard and

place darts as close as possible to the centre of the target in order

to obtain a maximum number of points. Each session lasted 15

20 min and consisted of 6080 throws. At the end of the six weeks,

each subject had made more than 1200 throws. Before starting the

six-week training program and at the end of the six-week training

program, each subject performed a test with 15 throws. The mean

point obtained per dart was calculated by summing the number of

points of the 15 throws and then dividing by 15. Comparison of the

two scores provided an evaluation of the effect of training.

2.3. Electromyographic recordings (EMG)

The skin was prepared for EMG recordings obtained from paired

surface electrodes placed over the belly of the MD and BR muscles

of the right arm (see Fig. 1). A large reference electrode was placed

around the wrist. EMGs were recorded over a 250 ms time window

including 50 ms prior to the stimulus. EMG signals were amplified

(1000) with high pass filtering at 10 Hz and low pass filtering at

1 kHz before being sampled at 2 kHz by an A/D converter and

stored on a computer for off-line analysis.

2.4. Transcranial magnetic stimulation

A snugly fitting cap was positioned over the subjects head and

a grid was drawn with stimulus sites spaced 1.5 cm from the ver-

tex using the nasion-inion line and the inter-aural line as refer-

ences. TMS was delivered using a figure-of-eight coil with

external loop diameter of 9 cm connected to a MagStim 200 elec-

tromagnetic stimulator (maximum output intensity 2.0 T, Mag-

stim, Dyfed, UK). The coil was held tangentially to the skull

positioned at 45 in relation to the nasion-inion line with the han-

dle to the rear so that the induced monophasic current flow was in

a posterior to anterior direction. This is the most favorable orienta-

tion for activating the corticospinal tract transynaptically (Kanekoet al., 1996). The junction of the coil was placed over the site to be

stimulated on the left hemisphere that elicited MEPs in the right

contralateral target muscles.

2.5. Experimental protocol

Two sessions of identical measurements were carried out. The

first one was carried out before the training period (control) and

the second one at the end of the training period (six weeks later).

To record EMG activity, subjects were comfortably seated and

adopted a static position in order to produce constant low level

activity in each muscle. EMG activity was displayed on line on a

computer screen to allow the subject to maintain a constant and

stable low EMG activity set at 5% of the maximal EMG activity.Two sets of 2 s recordings were made to measure EMG activity,

154 F. Tyc, A. Boyadjian / Clinical Neurophysiology 122 (2011) 153162


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the first during low level activity produced during mapping and

the second during maximum voluntary contraction. The value of

the rectified EMG during low activity was divided by the values ob-

tained during maximal EMG activity to quantify the activity during

mapping. The mean values of the rectified EMG during low level

activity were stable at 5% of the maximal EMG activity in both ses-

sions. For MD recordings, the subject placed their arm in a stableposition aiming at a target to throw a dart. For BR, recordings were

obtained under two conditions. (1) Alone condition: the subject

maintained the 5% low activity in the BR muscle in a static position

with the forearm on an arm-rest. Particular care was taken to en-

sure that only the BR muscle was contracted and no EMG activity

could be recorded in the MD muscle as verified online at high mag-

nification on the screen. Mapping only started when the MD mus-

cle was silent. (2) Co-active condition: the subject maintained 5%

low EMG activity in both muscles (BR and MD).

2.6. Motor output mapping

Prior to mapping, the hot spot and the active motor threshold

(aMT) were determined for each muscle. The hot spot was the siteat which the largest MEP could be induced with suprathreshold

single stimuli applied with TMS. The aMT was defined as the low-

est stimulation intensity that induced a peak-to-peak MEP ampli-

tude of more than 200lV in 5 out of 10 trials in the target

muscle. The TMS intensity was then adjusted to 1.2 times the

aMT of each muscle for mapping. Three TMS response maps were

established on the left hemisphere: one for MD muscle and two

for BR muscle (Alone and Co-active condition). Four stimuli were

delivered at each grid site with intervals randomly ranging be-

tween 3 and 5 s. The four recordings were averaged and stored

on a computer for further off-line analysis.

2.7. Excitability curves

Excitability curves (Ridding and Rothwell, 1997) were obtained

by stimulating the BR hot spot with ten increasing TMS intensities

(from 1.2 to 1.65 aMT) under two conditions. Alone condition,

with only the BR muscle contracted and Co-active condition with

the two muscles (BR and MD) contracted. At each intensity, three

stimuli were applied and MEPs stored for further analysis.

2.8. Data analysis

To determine the cortical representation of each muscle the

four non-rectified EMG recordings were averaged for each stimula-

tion site. The peak-to-peak amplitude of the MEPs was measured

and plotted on medio-lateral and antero-posterior coordinates.

For each subject and for each muscle, a contour plot was drawnwith its external borderline corresponding to the amplitude of

the minimal MEP (2D representation). The area of the contour plot,

i.e. the muscle map representation on the scalp in cm2 was then

calculated.

For 3D representation, the Lorentzian 3D function was used to

fit data by the LevenbergMarquard nonlinear least-mean-square

algorithm (Press et al., 1986; Tyc et al., 2005; Devanne et al.,

2006). This algorithm determines the function parameters thatminimize the sum of the squared differences between the observed

and the predicted values of the dependent variable using a gradient

descent-based optimization procedure. Before fitting, the baseline

was adjusted to the mean rectified EMG activity recorded during

the 2 s low level activity. The Lorentzian equation relating the

peak-to-peak amplitude of the MEP and the antero-posterior (y)

and medio-lateral (x) coordinates was given by the following

equation:

ZZmax

1 xx0a

2 1 yy0

b

2

Zmax is the estimated amplitude of the maximal MEP that is located

at coordinates x0 and y0. The parameters a and b reflect the

straightness of the peak in the medio-lateral and antero-posterior

directions, respectively. It has been shown that the estimated coor-

dinates of the theoretical hot spot (x0 and y0) of each muscles rep-

resentation were within the area from which MEPs were evoked

and very close to the site at which the largest response was ob-

tained experimentally (Devanne et al. 2006).

For excitability curve fitting, we used the Boltzmann sigmoidal

function where MEPmax represents the plateau level, S50 the stim-

ulus intensity required to obtain the 50% plateau value, and k re-

flects the slope of the curve:

MEP MEPmax

1 ess50=k

For statistics a two-way ANOVA for repeated measurements

was calculated. Muscle representation variables (2D and 3D) and

the excitability curves were compared between sessions for both

muscles and between both conditions for BR muscle (Alone and

Co-active) using a paired t-test as appropriate. To test the effect

of independent variables on excitability curves, we used a t-test

based on the standard error of estimate associated with each

best-fit parameter in each subject. The level of significance was

set at 5%.

3. 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

Fig. 1. Photo showing the position of the throwing arm and the place of the electrodes on MD and BR muscles. Right, rectified EMG obtained during the three phases of

throwing. Note the co-activation of MD and BR muscles during throwing.

F. Tyc, A. Boyadjian / Clinical Neurophysiology 122 (2011) 153162 155


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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 mus-

cles. The aMT of the BR muscle expressed as a percentage of the

maximal stimulator output were 34.8 1.72% (mean SEM) before

the training program and 34 2.08% after training. For the MD

muscle the aMT were 37.7 2.69% and 37 2.21% before and after

the training program.

By stimulating M1 and recording the MEPs from the target mus-

cles, an estimate of the representation of each muscle was obtained

on the scalp. Fig. 2 is an example of the MEPs obtained for the MD

and BR muscle representations before and after six-weeks training

in one subject. The location of MEP traces on the grid corresponds

to the scalp position from which they were evoked. The same

Fig. 2. Mean of 4 MEPs produced by TMS in MD and BR muscles at each scalp position in one subject before and after the 6 weeks training session. The location of the MEP

traces on the grid corresponds to the scalp sites from where they were evoked. V, vertex position.



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protocol was applied to each subject. The data obtained for the six

subjects before and after training on MD muscle are provided in

Table 1. The mean number of sites from which a MEP could be in-

duced in the MD muscle increased from 13 to 17. The mean surface

area of the MD muscle representation containing the sites in-

creased significantly (p < 0.006) from 27 to 35 cm2 after training.

This modification is illustrated by the contour plots obtained in

one subject in Fig. 3A. After the training session the mean motor

area for the MD muscle represented 129% of the mean motor area

obtained before training.

For the BR muscle cortical map area, the interaction between ses-

sion (before and after training) and condition (Alone and Co-active)

was tested with two way repeated ANOVA. No statistically signifi-

cant interaction was found (F= 0.0546, P= 0.824). The BR muscle

representation was determined before and after training, as was

the representation of the MD muscle (Fig. 2). Training induced sim-

ilar increasesin the number of MEPs andmap area forthe BRmuscle

as was observed forthe MD musclerepresentation (Fig.3B).The size

of the surface area of the cortical representation of the BR after

training was significantly different from before training (p < 0.02).

The results are given in Table 2 for the six subjects (BR alone).

3.1. The effects of co-contraction

Mapping was performed to evaluate the effect of co-contraction

on the representation of the BR muscle (Fig. 2, BR Co-active). The

surface area of the BR representation increased during co-contrac-

tion as shown in Fig. 3C. Table 2 provides the results for the six

subjects (BR Co-active). The mean number of cortical sites from

which a MEP could be obtained on the BR muscle in the Co-active

condition was 19 compared to 16 in the Alone condition. The mean

BR muscle representation area was 39 cm2 in the Co-Active Condi-

tion and was significantly larger (p < 0.02) than the 31 cm2 when

the BR muscle was tested alone.

3.2. Dual effects of co-contraction and training

The effect of co-contraction of both muscles was measured on

the BR muscle representation before and after the training session.

Table 1

Map areas and number of MEPs for MD muscle for six subjects before and after the

6 weeks training. Means are shown SEM.

MD map area (cm2) Number of MEP

Before After % Before After %

1 37.1 47 127 15 22 147

2 21.2 34.9 165 12 16 133

3 32.3 35.9 111 17 17 100

4 22.4 26.4 118 11 14 127

5 22.6 30.7 136 12 16 133

6 27.4 32.1 117 13 17 131

Mean 27 2.6 35 2.9 129 8.0 13 0.9 17 1.1 128 6.3

Fig. 3. Cortical representations obtained in one subject for MD (A) and BR (B) muscles before (straight line) and after (dotted line) training. C and D, cortical representations ofBR muscle obtained in the Alone (arrows) and the Co-Active (dashed line) Conditions before training (C) and after training (D).



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One example obtained in one subject is shown in Fig. 3C and D

where an increase in the surface area of the BR muscle was ob-

served. Data for the six subjects are given in Table 2, confirming

the effect of co-contraction and the effect of training on the mean

surface area of BR muscle representation. The mean number of cor-

tical sites from which a MEP could be obtained on the BR in the Co-

Active Condition was 19 before training against 22 after training.

The 48 cm2 of the mean surface area of the BR muscle reached after

training must be compared to the 39 cm2 measured before train-

ing. The increase was significant (p < 0.02) and represented 122%

of the map area before training.

3.3. 3D representation of the MD and BR muscles

To estimate the coordinates (x0, y0) of the theoretical hot spots,

a 3D representation of the muscles was calculated in order to fol-

low the modification of the location of the hot spots in the three

experimental situations. Fig. 4A illustrates the modification ob-

tained on 3D representations after training for both muscles. It

indicates an increase in the cortical excitability associated with

an increase of the cortical surface from which the muscle could

be activated. The mean R2 values were between 0.71 and 0.84 for

the six subjects. The distances between the theoretical hot spots

of the MD and the BR (Table 3) were significantly different

(p < 0.03) in the Alone Condition but not in the Co-Active Condition

(p < 0.06). For one subject fig. 4B (left) shows that the co-contrac-

tion induced a reduction of the inter-spot distance from 18 to

7.5 mm before training. After training, the inter-spot distance

was 4.1 mm for the BR alone while the location of the hot-spots

nearly coincided (0.5 mm) in the Co-Active Condition. The histo-

grams in Fig. 4B (right) show the differences in inter-spot distances

between before and after training. In the Alone Condition a reduc-

tion of the inter-spot distances was observed in five out of six sub-

jects and in all subjects in the Co-Active Condition. The reduction

emphasizes the dual effect of training and co-contraction.

3.4. Excitability curves

The excitability curves measured on the BR muscle showed an

increased MEP area when the stimulation intensity was increased

before and after the training session under the Alone and Co-Active

Condition (Fig. 5, left). During co-activation, the plateau levels ofthe curves reached higher values in each subject and for each

session compared to the levels reached when the BR muscle was

activated alone. The histograms of Fig. 5 (right) confirm that the

values of the plateau levels obtained from the excitability curves

before and after training for the six subjects were systematically

and significantly higher during co-contraction (142% and 159% be-

fore and after training). The increase in cortical excitability re-

sulted from the combined effects of training and co-contraction.

4. 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 rep-resentations of the co-contracted muscle.

4.1. Condition of recordings

At rest, proximal muscles are difficult to map (Levy et al., 1991;

Amassian et al., 1995). Stimulus intensitycan reach 80%of the max-

imal intensity of the stimulator that is approximately twice the

intensity used during low level activity (Tyc and Boyadjian, 2006).

In contrast, when a muscle is slightly activated, the MEP threshold

is decreased and TMS mapping is facilitated (Wilson et al., 1995).

Our experimental protocol relies on these observations.

4.2. Location of training-dependent plasticity

The increase of MEP size induced by co-activation and training

reflects a modification of the excitability of the cortico-spinal sys-

tem as a whole without providing evidence that plasticity occurs at

cortical levels. However, it can be argued that the observed effects

on corticomotor excitability cannot exclusively operate at the

spinal level even though the spinal neuronal circuitry has been

shown to exhibit adaptive plasticity in experimental animals

(Wolpaw and Carp, 1993) and in humans (Baylor and Benjuya,

1989). Because TES produces a greater proportion of direct activa-

tion of corticospinal neurons than TMS (Day et al., 1987a, b;

Rothwell, 1997) and because training induces an increase in MEPs

evoked by TMS but not by TES brain stem or cervical stimulation

(Classen et al., 1998; Muellbacher et al., 2001; Perez et al., 2004;

Garry et al., 2004), this form of plasticity is more likely to occurat the level of the cortical networks than at subcortical levels.

Table 2

Map areas and number of MEPs for BR muscles of six subjects before and after the 6 weeks training in the two conditions: Alone (only BR muscle contracted) and Co-Active (BR

and MD muscles co-contracted). Means are shown SEM.

BR Alone BR Co-Active % Co-Active/Alone

Before After % Before After % Before After

Map area (cm2)

1 38.4 58.8 153 54.5 60.1 110 142 102

2 31.7 39.3 124 34.5 42.6 123 109 109

3 39.1 42.8 110 41.2 50.3 122 105 118

4 28.6 40.3 141 39.9 54.5 137 140 135

5 24.8 29.8 120 31.3 34.6 111 126 116

6 25.3 32.6 129 34.1 44.9 132 135 138

Mean 31 2.6 41 4.2 129 6.3 39 3.4 48 3.7 122 4.4 126 6.4 120 5.8

Number of MEP

1 17 25 147 22 26 118 129 104

2 17 20 118 17 23 135 100 115

3 19 20 105 20 21 105 105 105

4 16 19 119 19 24 126 119 126

5 13 15 115 15 18 120 115 120

6 14 18 129 18 20 111 129 111

Mean 16 0.9 20 1.3 122 5.8 19 1.0 22 1.2 119 4.4 116 4.9 113 3.5



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4.3. Reproducibility of cortical M1 maps

Although there can be no doubt that the brain displays plastic-

ity, stability of cortical networks is also needed, as discussed in a

recent review by Wandell and Smirnakis (2009).

That motor cortical map representations are reproducible insubjects over a long period of time is well documented. The

TMS-mapped representations of two intrinsic hand muscles were

found to be very reproducible when mapping was repeated after

intervals of up to 181 days (Wilson et al., 1993). A method for

mapping the motor cortex by TMS was tested statistically for its

reproducibility and found to be reliable for mapping the human

motor cortex (Mortifee et al., 1994). Maeda et al. (2002) investi-gated the reproducibility of mapping techniques on six normal

Fig. 4. (A) Three-dimensional reconstructions of MD and BR muscles based on MEP recordings before and after training. The total variance accounted for by fitting the

Lorentzian function to the data points is given by the R2 value. (B) Left, the diagrams illustrate the measure of the distance between MD and BR hot spots in one subject chosen

to illustrate the maximal reduction of the inter-spot distances. Right, the histograms represent the differences between inter-spot distances before and after training in the

two conditions for the six subjects.



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volunteers, each studied on two occasions several weeks apart

(ranging from 21 to 132 days) and showed a low degree of variabil-

ity of repetitive TMS (rTMS) effects in the human brain. The areas

of the scalp from which responses were evoked from corticospinal

cells projecting to three intrinsic hand muscles were systematically

mapped using TMS on eight normal subjects at different intervals

(24 h, one week and two weeks). The area, volume, and centre

of gravity of these maps did not change significantly over that per-

iod. It was concluded that TMS mapping is suitable for studies that

aim to examine the effect of various interventions on the cortical

representation of individual muscles in human subjects (Miranda

et al., 1997; Uy et al., 2002.; Pitcher et al., 2003; Monfils et al.,

2005). Variation in the response to TMS in the general population

allowed Wassermann (2002) to state with confidence that the MEP

to single and paired TMS is a sensitive measurement of the cortico-

spinal function. Taken together, and even though some differences

in aMT and cortical excitability exist between subjects, these find-

ings demonstrate that cortical maps are reproducible in a given

subject over long periods of time and are similar in both hemi-

spheres, and are similar in left- and right-handed subjects. The sta-

bility of aMT observed in our experiments between the twosessions validates our choice to consider the first session of mea-

surements before training as the control condition, as well as our

use of map parameters for investigation of long-term effects of

training.

4.4. A cortical representation of coordination?

The capacity of M1 to undergo plastic reorganization following

skill acquisition and training is well established in humans and

animals (Pascual-Leone et al., 1994, 1995; Classen et al., 1998; Kar-

ni et al., 1998; Kleim et al., 1998; Liepert et al., 2000; Plautz et al.,

2000; Yahagi and Kasai, 1998; Muellbacher et al., 2001; Tyc and

Boyadjian, 2006.). Many studies have investigated the effect ofshort-term training on the cortical representation of distal muscles

executing repetitive sequences of finger movements (Tyc and Boy-

adjian, 2006). For example, in normal human subjects instructed to

practice a repetitive sequence of finger movements, the amplitude

and extent of finger muscle representation assessed by TMS in-

creased in M1 contralateral to the performing hand as the speed

of performance increased over a single day of training (Pascual-

Leone et al., 1994). In contrast, we focus our experiments on the ef-

fects of a six-week training period on the cortical representation of

a complex coordinated movement namely the movement executed

by a subject playing darts, in which all the joints in an upper limb

are involved in a specific coordination pattern and timing of prox-

imal and distal muscles (Temprado et al., 1997; Scott, 2000).

Motor patterns at each joint must be carefully coordinated to

smoothly move the joints and the hand through space. Many stud-

ies have described the trajectories of hand and arm movements un-

der normal conditions as straight hand paths called stereotyped

movements (Bernstein, 1967; Flash and Hogan, 1985; Wolpert

et al., 1995). These were defined as simple basic motor elements

(primitives). The notion that skilled movements might reflect a

process for the concatenation of consecutive movement elements

into complex movements was suggested by Sosnik et al. (2004).

On this assumption, a new primitive movement could be generated

by training which would be different from the sum of the elements

that comprised the sequence of initial movements (Engel et al.,

1997). By studying the acquisition of skilled motor performance,

Karni et al. (1995, 1998) showed that performance was paralleled

by the emergence of a more extensive representation of a trained

sequence of movements in M1. It has been suggested that a specificrepresentation of the sequence might be implemented at the M1

level as a new functional unit, differentially from the component

movements (Karni et al., 1998). In monkeys, practice-dependent

changes in the functional topography of M1 were reported by Nudo

Table 3

Distances (mm) between estimated hot spot of MD and BR muscles before and after

training in the two conditions (Alone and Co-active) for the six subjects. These data

were used to measure the differences between inter-spot distances represented in

Fig. 4B right.

Distance between MD and BR hot spot

Alone Condition Co-Active Condition

Before After Before After

1 20.0 18.1 22.7 14.2

2 18.0 4.1 7.5 0.5

3 10.4 11.5 11.7 11.3

4 15.3 9.8 14.2 11.3

5 15.5 7.2 15.3 10.4

6 15.3 13 13.2 8.8

Mean 15.7 10.6 14.1 9.4

Fig. 5. (A) Excitability curves obtained on the BR muscle hot spot for one subject before and after training in the two conditions Alone (straight line) and Co-Active (dotted

line). (B) Histograms representing the values of the plateau obtained on the excitability curves before and after training in the two conditions for the six subjects. Note the

different scale for subject number 3 on the right (ordinates). * indicates a significant difference (p < 0.05) in the plateaus reached in the Alone and Co-Active conditions;** indicate a significant difference (p < 0.05) in the plateaus reached before training and after training.



9/10

et al. (1996, 2001). After a few weeks of training on a task that re-

quired skilled manipulation, a new movement representation was

observed in M1 that was not found in untrained brains. These find-

ings support the idea of a cortical representation of the learned

motor sequence in M1 and underpinned our experimental

protocol.

Our finding that the co-activation of the proximal and the distal

muscles enhanced the TMS-evoked motor output in the distal BRmuscle showed that some functional networks were triggered dur-

ing coordinated movements. We interpreted the enlargement of

the motor cortical output maps to the muscles involved in the task

and their overlap indicative of a functional link between the two

target muscles carrying out the coordination. Our observation that

the proximal muscle modified the excitability curves of the distal

muscle confirmed that the sharing of networks is necessary for

coordination, as observed in other studies (Devanne et al., 2002;

Ginnaneschi et al., 2006).

TMS studies have shown that the cortical representations of dif-

ferent muscles overlap on M1 (Wilson et al., 1993; Wassermann

et al., 1993; Liepert et al., 1999; Tyc et al., 2005; Devanne et al.,

2006). In animals, studies involving the superposition of M1 topo-

graphical maps obtained by micro-stimulation, have shown that

motor cortical zones controlling different forelimb segments are

interconnected by intrinsic horizontal collaterals (Capaday et al.,

1998; Huntley and Jones, 1991; Keller, 1993; Rioult-Pedotti and

Donoghue, 2003; Tokuno and Tanji, 1993). In Rhesus monkeys,

Park et al. (2001) found regions combining both distal and proxi-

mal muscles following electrical stimulation of the cortical surface.

In the cat, simultaneous stimulations of two cortical points were

additive and resulted in a new movement that was a combination

of the movements elicited by stimulation of each point on its own

(Ethier et al., 2006). Brain imaging or TMS have shown that arm or

hand movements were triggered by large areas of the motor cortex

(Amassian et al., 1995; Devanne et al., 2002; Hallet, 2000; Kobay-

ashi and Pascual-Leone, 2003; Sanes et al., 1995; Schieber and Hib-

bard, 1993; Walsh and Cowey, 2000 Schieber, 2001). These

findings suggest that widely distributed motor cortical territoriesare functionally linked during coordinated movements. Whether

the expansion of the muscle representations in M1 observed in

the darts players can be related to the development of a functional

unit remains a matter of speculation. However, the highly distrib-

uted organization of M1, convergence, divergence and horizontal

connections with wide overlapping territories of different muscles,

makes the hypothesis of a cortical representation of movement

coordination plausible.

Acknowledgements

We thank our students for giving their time to participate in

this study. We thank Professor A.R. Lieberman for editing our man-

uscript and correcting the English language. We are grateful to Pro-

fessor John C. Rothwell for his advice.

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