Increased muscle activation following motor imagery during the rehabilitation of the anterior cruciate ligament.

Abstract

Motor imagery (MI) is the mental representation of an action without any concomitant movement. MI has been used frequently after peripheral injuries to decrease pain and facilitate rehabilitation. However, little is known about the effects of MI on muscle activation underlying the motor recovery. This study aimed to assess the therapeutic effects of MI on the activation of lower limb muscles, as well as on the time course of functional recovery and pain after surgery of the anterior cruciate ligament (ACL). Twelve patients with a torn ACL were randomly assigned to a MI or control group, who both received a series of physiotherapy. Electromyographic activity of the quadriceps, pain, anthropometrical data, and lower limb motor ability were measured throughout a 12-session therapy. The data provided evidence that MI elicited greater muscle activation, even though imagery practice did not result in pain decrease. Muscle activation increase might originate from a redistribution of the central neuronal activity, as there was no anthropometric change in lower limb muscles after imagery practice. This study confirmed the effectiveness of integrating MI in a rehabilitation process by facilitating muscular properties recovery following motor impairment. MI may thus be considered a reliable adjunct therapy to help injured patients to recover motor functions after reconstructive surgery of ACL.

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Applied Psychophysiology and
Biofeedback
In association with the Association
for Applied Psychophysiology and
Biofeedback

ISSN 1090-0586
Volume 37
Number 1

Appl Psychophysiol Biofeedback (2012)
37:45-51
DOI 10.1007/s10484-011-9175-9
Increased Muscle Activation Following
Motor Imagery During the Rehabilitation
of the Anterior Cruciate Ligament
Florent Lebon, Aymeric Guillot &
Christian Collet

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Increased Muscle Activation Following Motor Imagery During
the Rehabilitation of the Anterior Cruciate Ligament
Florent Lebon•Aymeric Guillot•Christian Collet
Published online: 30 November 2011
? Springer Science+Business Media, LLC 2011
Abstract
of an action without any concomitant movement. MI has
been used frequently after peripheral injuries to decrease
pain and facilitate rehabilitation. However, little is known
about the effects of MI on muscle activation underlying the
motor recovery. This study aimed to assess the therapeutic
effectsofMIontheactivationoflowerlimbmuscles,aswell
as on the time course of functional recovery and pain after
surgery of the anterior cruciate ligament (ACL). Twelve
patients with a torn ACL were randomly assigned to a MI
or control group, who both received a series of physio-
therapy. Electromyographic activity of the quadriceps, pain,
anthropometrical data, and lower limb motor ability were
measured throughout a 12-session therapy. The data pro-
vided evidence that MI elicited greater muscle activation,
eventhoughimagerypracticedidnotresultinpaindecrease.
Muscle activation increase might originate from a redistri-
bution of the central neuronal activity, as there was no
anthropometric change in lower limb muscles after imagery
practice. This study confirmed the effectiveness of inte-
grating MI in a rehabilitation process by facilitating
Motorimagery(MI)isthementalrepresentation
muscular properties recovery following motor impairment.
MI may thus be considered a reliable adjunct therapy to help
injured patients to recover motor functions after recon-
structive surgery of ACL.
Keywords
Electromyography ? Motor rehabilitation
Motor imagery ? Anterior cruciate ligament ?
Introduction
The anterior cruciate ligament (ACL) torn is one of the most
serious injuries that might occur during sporting activities
(Derscheid and Feiring 1987; Roos et al. 1995). Recon-
structive surgery is usually well-adapted in case of severe
injury of the ACL to reconstruct the ligament with different
techniques including hamstring or patellar tendon graft
(Lemaire or Kenneth Jones techniques) before a long period
of physical rehabilitation. However, the effects of post sur-
gicalpainandeffusion,combinedwithdecreasedfunctionof
the knee, result in reduced muscle activation in the early
recovery from ACL surgery. Therefore, the combination of
thesefactorsaftersurgeryresultsinmuscleatrophyandforce
loss, especially in the quadriceps muscle. For instance,
Hortobagyi et al. (2000) reported a 47% quadriceps strength
lossafterinjury,albeitwithonly11%duetotheamyotrophy.
Immobilization is therefore likely to primarily affect the
neural factors at the peripheral level (Ha ¨kkinen 1994;
Kaneko et al. 2003). Functional changes may also occur at
thecentrallevelasthemotorcortexisreorganizedduringthe
motionless period (Liepert et al. 1995). Motor imagery (MI)
is a cognitive process during which the representation of an
action is mentally reproduced without any overt motor out-
put(Jeannerod1995).DifferenttypesofMIcanbedescribed
and easily combined. While people commonly report that
F. Lebon
Applied Clinical Neuroscience, Neurology Research Group,
Department of Medicine, Centre for Brain Research, University
of Auckland, 1142 Auckland, New Zealand
A. Guillot ? C. Collet (&)
Centre of Research and Innovation in Sport, EA 647, Mental
Processes and Motor Performance, University Claude Bernard
Lyon I, University of Lyon, 27-29 Boulevard du 11 Novembre
1918, 69622 Villeurbanne, France
e-mail: christian.collet@univ-lyon1.fr
A. Guillot
Institut Universitaire de France, 103 Boulevard Saint-Michel,
75005 Paris, France
123
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DOI 10.1007/s10484-011-9175-9
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usingvisualimageryandauditoryimagery(forexample,the
rate and pace at which the movement is executed), kinaes-
thetic imagery is defined as the set of sensations that match
those generated during the execution of the movement, such
as muscle tension, range of motion… More generally, it is
built on proprioceptive cues (Kosslyn et al. 1990). Although
MI can involve selectively specific sensory information, it
often combines several indices from different sensory sys-
tems, thus making MI a global sensory-motor experience, in
reference to perception. This technique has been shown to
substantially enhance motor rehabilitation, as well as
increase self-confidence and motivation of injured patients
(e.g., Cramer et al. 2007). Studies demonstrated that imple-
menting MI during the classical course of physical therapy
resulted in less anxiety and pain, assessed by questionnaires
andinterviews(Driedigeretal.2006;Evansetal.2006;Law
etal.2006;Milneetal.2005;Sordonietal.2000),andfurther
facilitated motor function recovery following sport injuries
(Christakou and Zervas 2007; Christakou et al. 2006; Cupal
andBrewer2001;Green1992;Heil1993;IevlevaandOrlick
1991; Richardson and Latuda 1995; Sordoni et al. 2002;
Taylor and Taylor 1997). To the best of our knowledge, the
study by Cupal and Brewer (2001) was the only research
focusing on the effect of MI after ACL injury. The main
outcomemeasureswerekneestrength,re-injuryanxiety,and
pain. The results showed greater knee strength and less
re-injuryanxietyandpainforthetreatmentgroupat24 weeks
post-surgery than for placebo and control group participants.
The authors concluded that relaxation and imagery sessions
facilitated motor recovery after ACL reconstructive surgery.
However, measurements were recorded 24 weeks after the
surgery. It would have been interesting to assess muscle
activation during the first weeks post-surgery to explain the
mechanisms of these effects in greater details.
Based on the results mentioned above, the purpose of
the present study was to assess the therapeutic effects of MI
on electromyographic (EMG) activity, functional recovery,
range of motion (ROM), and effusion resorption, as well as
pain management, in athletes who have undergone
arthroscopic ACL reconstructive surgery. We hypothesized
that a guided MI training program would contribute to
improve motor recovery by increasing muscle activation
and decreasing pain.
Methods
Participants
Twelve volunteers (10 men and 2 women), aged from 18 to
40 years (mean = 28.5 ± 5.0), gave their informed con-
sent to take part to a 5-week motor rehabilitation program.
The medical team was closely involved in the experiment
and the MI program content received the agreement of the
direction of the IRIS functional rehabilitation centre of
Lyon.
The criteria to include patients in the experimental
paradigm were clearly defined. All underwent a successful
arthroscopic ACL reconstructive Kenneth Jones-technique
surgery using a central one-third of patellar tendon graft.
None showed other acute lower extremity trauma (e.g.,
meniscal damage, micro-fracture, medial, lateral or pos-
terior cruciate ligament injury). Nine participants had
regular sporting competitive activity, from departmental to
national level. The patients incurred right ACL injury
while participating in soccer (n = 5), skiing (n = 3),
handball (n = 2) or other sport activities (n = 2). Personal
data related to individual technical characteristics of sur-
gery and to drug treatment were collected confidentially
from the medical files.
Dependent Variables
The data recordings of the test sessions are summarized in
Table 1.
Self-Estimation of Pain
The Visual Analog Scale (VAS) was used to assess pain,
before taking medication (Bodian et al. 2001). The patients
were requested to mark the perceived pain on an analog,
not graduated scale, representing the increasing pain from
the left to the right on a black line, 10 cm in length. The
back of this analog scale was a numeric scale allowing the
experimenter to change patient assessment into a numeric
value from 0 (no pain) to 10 (severe pain). This procedure
prevented the patient to attach too much importance to
numerical values. The VAS offered a quick assessment of
pain, with a high correlation with pain measurement using
verbal and numeric pain-rating scales (Ekblom and Hans-
son 1988). Reliability and validity were previously
addressed (Badia et al. 1999; Hoher et al. 1995).
EMG Recordings
The activation of the right and left vastus medialis was
recorded using surface EMG electrodes positioned on the
belly of the muscles (YSY Est Evolution, France) during a
maximal extension of the knee. Circular electrodes with a
diameter of 10 mm were placed with reference to con-
ventional international recommendations (Hermens et al.
2000).
While sitting on a chair with both arms on the chest, the
participants were instructed and verbally encouraged to
perform two isometric maximal voluntary contractions
(iMVC), with the knee in full extension. The best attempt
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was kept for data processing, with a 5-min rest between the
2 contractions. Trials of the non-injured limb were first
attempted. Raw EMG signals were sampled at 2,048 Hz
before being processed. Then, the signal was filtered
(Butterworth order 4, band pass 10–500 Hz), and the root
mean squared-value (EMG rms) was calculated using a
25 ms average time period. Before placing the EMG sur-
face sensors, the skin was shaved, abraded and cleaned
with alcohol swabs to improve the contact with the skin but
also to limit skin impedance. After each electrode place-
ment, manual muscle testing was performed to ensure the
placement and appropriate related EMG signal. Electrode
positioning was marked each time, to guarantee the accu-
racy of EMG recordings during each test sessions (test and
retest). EMG data were processed to test whether MI
training elicited increase and improvement of muscle
activation during the pre- and the post-tests and during the
intermediate sessions, i.e., sessions 4, 7 and 10. EMG
recordings were also used as control procedure during
mental training to check that the participants have not
associated muscle contraction—even tonic activity—while
mentally rehearsing.
Motor Ability of Lower Limb
The patients completed the Lower Extremity Functional
Scale (LEFS—Binkley et al. 1999) to evaluate their ability
to perform daily activities with their injured lower limb.
The version of the scale consisted of 20 items. The intro-
ductory statement of the questionnaire states: ‘‘Today, do
you or would you have any difficulty at all with:’’ followed
by a listing of the functional items (Binkley et al. 1999,
p. 74). Test–retest reliability is high, i.e., 0.98 and 0.88,
when tested by both Watson et al. (2005) and Yeung et al.
(2009), respectively. The LEFS is also responsive to clin-
ical changes as shown by both studies. The participants
filled out the questionnaire and rated from 0 (Extreme
Difficulty or Unable to Perform Activity) to 4 (No Diffi-
culty) the trouble they would have encountered if they had
to perform the movement physically. The maximal score
could thus be 80. Three other intermediate levels were
proposed, ‘‘Quite a Bit of Difficulty’’ (level 1), ‘‘Moderate
Difficulty’’ (level 2) and ‘‘A Little Bit of Difficulty’’ (level
3). The 5-point difficulty rating scale was selected to
maximize the capacity of the scale to measure change.
Anthropometrical Data
Anthropometrical data of the injured leg were measured to
be compared with the non-injured side, and to assess the
magnitude of effusion resulting from surgery and amyot-
rophy: (1) knee circumference was measured just above the
patella, (2) thigh circumference was measured 15 cm from
the superior edge of the patella, and (3) ROM of the knee
was assessed with a goniometer. All data were collected by
the same experimenter to prevent variability in the proce-
dures and ensure the validity of the measurement. Sensor
placement and MI sessions were nevertheless performed by
two different experimenters in order to make the assessors
blind to condition.
Procedure
The participants were recruited on a rolling basis when
they received the surgery diagnostic. The criteria for
inclusion in the study were: (1) to have undergone surgery
within a 6-month period, i.e., the duration of implementa-
tion of the experimental protocol, (2) to present an isolated
rupture of the ACL and (3) to benefit from reconstructive
surgery with the patellar tendon. Twelve patients fulfilling
these conditions were included in the sample after they
gave their informed consent. Each was randomly assigned
in the MI group (7 patients) or in the control group
(CTRL—5 patients). All initiated the rehabilitation pro-
gram within a period of 7–12 days after surgery (mean =
8.1 ± 2.39).
The MI rehabilitation program ranged from 28 to
34 days (mean = 30 ± 2.02). Each participant underwent
a total of 12 sessions. The sessions were arranged every
2 days with every session lasting 15 min (whenever pos-
sible, as a function of the schedule of each patient).
Both groups received traditional rehabilitation sessions
simultaneously (a 30-min every 2 days) with strengthen-
ing exercises,massages,passive jointmobilization,
Table 1 Time-table of physiological and psychological recordings
Session1: pre-testSession 4Session 7 Session 10Session 12: post-test
EMG activity
Anthropometric data
Pain
LEFS test
EMG activityEMG activity
Anthropometric data
Pain
EMG activityEMG activity
Anthropometric data
Pain
LEFS test
During every test session, electromyographic (EMG) activity was recorded. Anthropometric data, including knee effusion and thigh circum-
ference, were also considered as dependent variables. The Lower Extremity Functional Scale (LEFS) evaluated the individual ability of injured
participants to perform twenty daily activities
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electrostimulation, cycling without strain and cryotherapy.
The control group did not perform any mental training
based on movement, but was subjected to a neutral task
(e.g., mental calculation or crosswords) during equivalent
time along the physical therapy.
Motor Imagery Training
The instructions were designed to make the patients using
kinesthetic imagery rather than pure visual MI. Kinesthetic
imagery is more likely to provide better somesthetic bio-
feedback from joint and muscles (Hale 1982; Ranganathan
et al. 2002) and to better increase corticomotor excitability,
primarily at the supraspinal level (Stinear et al. 2006).
During the MI sessions, the participants were sited with the
legs extended to preserve physiological activation, favor-
able to MI efficiency (Holmes and Collins 2001). As sug-
gested by Rushall and Lippman (1998) and Louis et al.
(2011), relaxation is not essential to MI training, and may
even limit its benefits when the ultimate imagery outcome
is to improve learning and motor performance. In other
words, relaxation was only used during initial imagery
sessions to help the participants to reduce interferences
from distractions just before using MI, but they were then
requested to increase their arousal level as they would do
during physical performance (Guillot and Collet 2008;
Louis et al. 2011). The participants were instructed to
perceive muscle contractions and joint tension while
imagining maximal isometric contraction of a full knee
extension during 10 s, without moving. Each participant
was thus clearly instructed not to contract their muscle
during MI sessions. They performed 3 blocks of 10
imagined contractions, with a 10-s rest period between
rehearsals and 2-min rest period between blocks. The
physiotherapists who undertook the physical care were
blinded to the first part of the session (i.e., MI or neutral
cognitive task). To check whether the participants did not
contract their muscles during MI trials, EMG recordings
were performed continuously during training.
Data Analysis
Due to the number of participants and as the distribution
was not Gaussian, only non-parametric tests were per-
formed. The EMG rms of the injured limb was normalized
to the contralateral healthy limb values to allow compari-
son between them, i.e., within-subject comparison. First,
the Mann and Whitney test compared both groups during
the pre-test. The Wilcoxon signed-ranks test was carried
out to compare the evolution of the dependent variables
during test sessions (Sessions 1, 4, 7, 10 and 12). The effect
sizes (ES) with 95% confidence intervals (CIs) were also
calculated using Cohen’s d (Cohen 1988) on the mean
difference between pre- and the post-rehabilitation periods.
The results are presented as mean (standard deviation), and
the alpha level was set at P\0.05.
Results
EMG Activity
First, the pre-test normalized EMG activity was similar in
the MI and the CTRL groups (Z = -0.24, P[0.05), data
being 9.11 (6.74) and 8.10 (5.54), respectively. Even
though both groups showed an increased in the muscular
activity at the end of the recovery therapy, the Wilcoxon
test revealed a significant difference between MI and
CTRL groups during the last test session (Z = -2.35,
P = 0.02, Fig. 1), normalized activity being 85.36 (28.12)
and 51.56 (18.81), respectively.
Pain
A significant pain decrease was observed between S1 and
S12 in both groups, but there was no group significant dif-
ferenceatthelastsession,meanscorebeing0.21(0.39)inthe
MI group and 1.20 (1.25) in the CTRL group (Z = -1.54,
P[0.05, NS; ES (d) = 0.03, trivial effect, [-1.05, 1.12]).
Anthropometric Measures
Increased ROM of the knee was measured in the MI and
CTRL groups, the respective difference between the last
and the first session being 37.86? (14.10) and 30.00? (7.91).
The difference did not reach significance (Z = -0.99,
Fig. 1 Increase in normalized electromyographic (EMG) activity
along the time course of the experiment (from Session 1 to Session
12). EMG activity of the vastus medialis of the injured limb was
normalized to EMG of the contralateral limb. EMG activity in the
motor imagery (MI) group was significantly higher during the last
session than that recorded in the control (CTRL) group. *P\0.05
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P[0.05, NS), but the effect size was large (ES (d) = 0.8,
[-0.4, 1.9]).
The data related to the effusion reduction did not reveal
significant group difference (Z = -0.51, P[0.05, NS),
mean differences between the circumference of the injured
and the contralateral knee being 0.93 cm (1.17) and 1 cm
(0.77) in the MI and CTRL groups, respectively (large
effect size, ES (d) = 0.7, [-1, 1.16]).
Finally, measures of the thigh circumference during the
last session provided evidence of a significant muscle
amyotrophy in both groups, even though the group differ-
ence was not significant (Z = -0.49, P[0.05, NS). The
mean amplitude of the circumference decrease was
1.57 cm (2.30) in the MI group and 2.25 cm (1.90) in the
CTRL group (small effect size, ES (d) = 0.3 [-0.8, 1.4]).
LEFS Scores
No significant difference was observed between the two
groups (Z = -0.274, P[0.05, NS). The mean score
during the last session was 49.00 (7.82) in the MI group
and 48.80 (10.70) in the CTRL group (small effect size, ES
(d) = 0.28 [-0.8, 1.4]).
Discussion
The main result of this study showed that muscle activation
increased from the pre- to the post-test in both groups, and
the activity was significantly greater in the MI group after
the rehabilitation program, than in the control group. These
data support previous findings demonstrating the effec-
tiveness of MI on strength gain (Yue and Cole 1992;
Ranganathan et al. 2004) and on the limitation of force loss
after immobilization (Newsom et al. 2003). However, the
relationship to muscle strength and EMG activity was not
established in this study. Despite the limitation of surface
EMG to examine muscle force (due to muscle factors,
recordings and analysis components, see Dowling 1997),
the greater increase in EMG activity following MI training
might be related to central activation modulation. Based on
the functional equivalence between MI and motor perfor-
mance (Decety et al. 1994; Lotze et al. 1999), and the
similar cortical reorganization following MI and physical
training, Ranganathan et al. (2004) explained the increase
in the elbow flexor and digiti minimi adductor muscles’
strength after MI by the enhancement of the cortical output
signal, which could drive the muscles to higher activation
level.
Moreover,theassociationofstrengthlossanddecrease in
the pattern of EMG activity with immobilization was highly
correlated to muscle activation level. Mizner et al. (2005)
reported that patients who underwent knee arthroplasty had
profound impairment of quadriceps strength 1 month after
surgery, due to their impossibility to command the muscle
activation voluntarily, as the joint remained immobilized.
To a lesser extent, this was also influenced by muscle
amyotrophy. By monitoring neuromuscular changes of the
knee extensors early after ACL reconstruction, Drechsler
et al. (2006) observed that the restoration of voluntary
activation was achieved by 3 months after surgery in most
cases. Nevertheless, the muscle weakness often persisted.
Electrophysiological data (EMG median frequency and
amplitude) suggested changes in the patterns of activation
andmotorunitsrecruitmentoflarge,fastcontractingmuscle
fibers, 1 and 3 months after surgery.
The evolution of the EMG activity during the rehabili-
tation period revealed a larger increase in the MI group as
compared to the CTRL group after the 7th MI session. The
use of kinesthetic MI might have influenced the modulation
of these physiological properties, hence resulting in higher
EMG activity. As shown by Stinear et al. (2006), kines-
thetic MI, but not visual MI, modulates the corticomotor
excitability,primarily at
instructions should therefore be carefully controlled before
engaging in MI to ensure its effectiveness in enhancing
motor recovery.
While imagery has been extensively, albeit not system-
atically, found to manage and decrease pain (e.g., Cupal and
Brewer 2001; Driediger et al. 2006; Evans et al. 2006; Law
et al. 2006, see also Moseley 2006; Moseley et al. 2008), the
present study failed to replicate this result. At first glance,
these findings seem somewhat inconsistent, and might be
due to the content of the MI scripts, which primarily
focused on motor recovery processes, and only integrated
pain management during the first sessions. Moreover, the
participants received strong analgesic treatments during
the first week following surgery, hence possibly limiting the
effect of mental practice on pain management. It was
therefore difficult to interpret the lack of MI effect, as the
self-evaluation by the patients may have been directly
biased by the medical analgesic treatment. Somehow, the
absence of significant difference strengthened the higher
level of EMG activity in the MI group, which did not
depend on lower pain during voluntary contractions.
As expected, the quadriceps size changed along the
rehabilitation period, i.e., its circumference decreased
similarly in both groups due to muscle atrophy. This result
confirms that MI may influence neural but not structural
modulations (Ranganathan et al. 2004; Zijdewind et al.
2003). Yue and Cole (1992) stated that strength gain fol-
lowing MI training was associated with increase in EMG
activity which was dependent upon changes in motoneu-
rons, interneurons and reflex pathways activities. MI
practice activates motor cortex areas (Decety et al. 1994;
Lotze et al. 1999) and facilitates the excitability of neural
thesupraspinallevel. MI
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pathways (Stinear et al. 2006), hence resulting in enhanced
motor reconstruction, without any effect on muscle size.
Furthermore, these data support the results by Christakou
and Zervas (2007) who did not found any MI effect on
effusion resorption and ROM following ankle sprain.
These two variables are highly correlated, the joint
amplitude being limited by the effusion. However, the
sample size was probably the main limitation of our study
and may have limited the effect of MI although the large
ES recorded for changes in ROM and effusion reduction
might suggest a reliable effect.
Conclusion
This study demonstrates that classical course of physical
therapy combined with MI could better enhance muscle
activation following ACL reconstructive surgery. Specifi-
cally, MI might influence the recovery of muscle activity,
thus supporting the MI efficiency on strength gain and lim-
itation of force loss after immobilization. MI should thus be
considered a reliable and cost-effective complement to
improve the process of functional rehabilitation. Joint
amplitude and stability remain the two crucial points on
which imagery should ideally be focused. Muscle properties
would then be better considered during motor recovery,
especially for injured athletes. Finally, imagining the
movement should ideally be performed during early stages
of the rehabilitation process (pre- and post-surgery) when
both passive and active motor executions are still limited by
the injury.
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