Post on 20-Apr-2023
“Neural and Muscular Determinants of Dorsiflexor Weakness in Chronic Stroke Survivors”
by Klein CS, Power GA, Brooks D, Rice CL
Motor Control
© 2013 Human Kinetics, Inc.
Note. This article will be published in a forthcoming issue of the
Motor Control. The article appears here in its accepted, peer-reviewed
form, as it was provided by the submitting author. It has not been
copyedited, proofread, or formatted by the publisher.
Article Title: Neural and Muscular Determinants of Dorsiflexor Weakness in Chronic Stroke
Survivors
Authors: Cliff S. Klein1,2
, Geoffrey A. Power3, Dina Brooks
1,2 and Charles L. Rice
3,4
Affiliations: 1Department of Physical Therapy, University of Toronto, Toronto, ON, Canada;
2Toronto Rehabilitation Institute, Toronto, ON, Canada;
3Canadian Centre for Activity and
Aging, School of Kinesiology, Faculty of Health Sciences, The University of Western Ontario,
London, ON, Canada; 4
Department of Anatomy and Cell Biology, Schulich School of Medicine
and Dentistry, The University of Western Ontario, London, ON, Canada.
Journal: Motor Control
Acceptance Date: March 15, 2013
©2013 Human Kinetics, Inc.
“Neural and Muscular Determinants of Dorsiflexor Weakness in Chronic Stroke Survivors”
by Klein CS, Power GA, Brooks D, Rice CL
Motor Control
© 2013 Human Kinetics, Inc.
Cliff S. Klein1,2
, Geoffrey A. Power3, Dina Brooks
1,2 and
Charles L. Rice
3,4
1Department of Physical Therapy, University of Toronto, Toronto, ON, Canada;
2Toronto
Rehabilitation Institute, Toronto, ON, Canada; 3 Canadian Centre for Activity and Aging, School
of Kinesiology, Faculty of Health Sciences, The University of Western Ontario, London, ON,
Canada; 4
Department of Anatomy and Cell Biology, Schulich School of Medicine and Dentistry,
The University of Western Ontario, London, ON, Canada
Abbreviated title: Post-stroke dorsiflexor weakness
Date of submission: March 8, 2013
Address correspondence and submit galley proofs to:
Cliff S. Klein PhD
Rehabilitation Institute of Chicago, 345 E. Superior St., Chicago, IL, USA, 60611
Phone:312-238-2695, cklein@ric.org
Geoffrey A. Power, School of Kinesiology, University of Western Ontario,
411D Arthur & Sonia Labatt Health Sciences Bldg, London ON, N6A 5B9
Phone: 519-661-2111 ext. 81628, geoffpowernl@gmail.com
Dina Brooks PhD, Dept of Physical Therapy, University of Toronto, 160-500 University Ave.,
Toronto, Ontario, M5G 1V7, Phone: 416-978-1739, dina.brooks@utoronto.ca
Charles L. Rice PhD, School of Kinesiology, University of Western Ontario,
411D Arthur & Sonia Labatt Health Sciences Bldg, London ON, N6A 5B9
Phone: 519-661-2111 ext. 81628, crice@uwo.ca
“Neural and Muscular Determinants of Dorsiflexor Weakness in Chronic Stroke Survivors”
by Klein CS, Power GA, Brooks D, Rice CL
Motor Control
© 2013 Human Kinetics, Inc.
Neural and muscular determinants of dorsiflexor weakness in chronic stroke survivors
Cliff S. Klein1,2
, Geoffrey A. Power3, Dina Brooks
1,2 and Charles L. Rice
3,4
1Department of Physical Therapy, University of Toronto, Toronto, ON, Canada;
2Toronto
Rehabilitation Institute, Toronto, ON, Canada; 3Canadian Centre for Activity and Aging, School
of Kinesiology, Faculty of Health Sciences, The University of Western Ontario, London, ON,
Canada; 4
Department of Anatomy and Cell Biology, Schulich School of Medicine and Dentistry,
The University of Western Ontario, London, ON, Canada
Abbreviated title: Post-stroke dorsiflexor weakness
Address correspondence to:
Cliff S. Klein PhD
Rehabilitation Institute of Chicago
345 E. Superior St.,
Chicago, IL, USA, 60611
312-238-2695
cklein@ric.org
“Neural and Muscular Determinants of Dorsiflexor Weakness in Chronic Stroke Survivors”
by Klein CS, Power GA, Brooks D, Rice CL
Motor Control
© 2013 Human Kinetics, Inc.
Abstract:
Few examined the contribution of neural and muscular deficits to weakness in the same stroke
subject. We determined maximal voluntary contraction (MVC) and 50 Hz torques, activation
(twitch interpolation), electromyographic (EMG) amplitude and antagonist coactivation, and
muscle volume using magnetic resonance imaging (MRI) of the dorsiflexors bilaterally in 7
chronic stroke subjects (40-67 y). Recordings of MVC and 50 Hz torque were also done in 7
control subjects (24-69 y) without stroke. The MVC torque was smaller in the contralesional
than ipsilesilesional limb (29.8±21.3 Nm vs. 42.5±12.0 Nm, P =0.04), and was associated with
deficits in activation (r2
=0.77) and EMG amplitude (r2
=0.71). Antagonist coactivation
percentage was not significantly different between limbs. Muscle volume, 50 Hz torque, and
specific torque (50Hz torque/muscle volume) were also not different between sides. The concept
that atrophy is commonplace after stroke is not supported by the results. Our findings indicate
that dorsiflexor weakness in mobile stroke survivors is not explained by atrophy or reduced
torque generating capacity suggesting an important role for central factors.
“Neural and Muscular Determinants of Dorsiflexor Weakness in Chronic Stroke Survivors”
by Klein CS, Power GA, Brooks D, Rice CL
Motor Control
© 2013 Human Kinetics, Inc.
Chronic stroke survivors (>1 y post-stroke) have varying degrees of weakness and
impaired motor control that compromises daily function (Arene & Hidler, 2009). During walking
the dorsiflexors help to stabilize the ankle during stance and optimize foot-ground clearance
during swing (Dubo et al., 1976). These dorsiflexion functions may be impaired by weakness
and thereby contribute to the slow gait and falls following stroke (Knutsson & Richards, 1979).
Weakness, defined as the inability to generate normal levels of torque during a maximal
voluntary contraction (MVC), predominates in the contralesional (paretic) limb after hemiparetic
stroke (Adams, Gandevia, & Skuse, 1990; Frontera, Grimby, & Larsson, 1997; Horstman et al.,
2008; Klein, Brooks, Richardson, McIlroy, & Bayley, 2010; Knorr, Ivanova, Doherty, Campbell,
& Garland, 2011; Landau & Sahrmann, 2002; Levin & Hui-Chan, 1994). Whether the loss of
strength arises solely from neural impairments or also reflects altered intrinsic muscle properties
is uncertain (Frontera, et al., 1997; Jakobsson, Edstrom, Grimby, & Thornell, 1991; Landau &
Sahrmann, 2002; Odajima, Ishiai, Okiyama, Furukawa, & Tsukagoshi, 1987; Ramsay, Barrance,
Buchanan, & Higginson, 2011; Scelsi, Lotta, Lommi, Poggi, & Marchetti, 1984; Slager, Hsu, &
Jordan, 1985).
Impaired muscle activation likely contributes to post-stroke weakness (Frontera, et al.,
1997; Horstman, et al., 2008; Klein, et al., 2010; Knorr, et al., 2011; Newham & Hsiao, 2001).
For instance, during a dorsiflexor MVC, the surface electromyographic (EMG) amplitude or
motor unit discharge rates of the tibialis anterior (TA) are often reduced in the contralesional
limb (Frontera, et al., 1997; Knorr, et al., 2011). In addition, activity of the antagonist muscles
during a MVC may reduce MVC torque. Antagonist coactivation in stroke survivors has been
shown to be excessive during an MVC in some cases (Klein, et al., 2010; Levin & Hui-Chan,
1994; Yusevich, 1968), although other reports show that coactivation is similar between the
“Neural and Muscular Determinants of Dorsiflexor Weakness in Chronic Stroke Survivors”
by Klein CS, Power GA, Brooks D, Rice CL
Motor Control
© 2013 Human Kinetics, Inc.
contralesional and ipsilesional limb (Clark, Condliffe, & Patten, 2006; Lum, Patten, Kothari, &
Yap, 2004; Newham & Hsiao, 2001; Wagner, Dromerick, Sahrmann, & Lang, 2007).
The contribution of post-stroke changes in muscle properties to dorsiflexor weakness is
uncertain (Frontera, et al., 1997; Jakobsson, et al., 1991; Landau & Sahrmann, 2002; Odajima, et
al., 1987; Slager, et al., 1985). The study by Landau and Sahrmann (2002) compared the side-to-
side differences in dorsiflexor MVC force and maximal force generating capacity evoked by 50
Hz stimulation over the TA. In the 14 subjects with chronic stroke, the mean MVC force was
significantly less in the contralesional than ipsilesional limb, but mean 50 Hz forces were not
different. However, contralesional 50 Hz force was 20-70% smaller than the ipsilesional value in
four persons, and was unexpectedly larger by 30-150% in five others, but the cause of these
differences was not evaluated (Landau & Sahrmann, 2002). A reduction in 50 Hz force may
result from muscle atrophy or reduced specific tension (ie., torque per unit area or volume), or
both, whereas an increase could indicate opposite responses. Post-stroke dorisflexor (Odajima, et
al., 1987; Ramsay, et al., 2011) or TA muscle fiber (Frontera, et al., 1997; Jakobsson, et al., 1991;
Scelsi, et al., 1984; Slager, et al., 1985) morphology has been determined, but the findings are
not always in agreement. One study reported smaller dorsiflexor cross-sectional area (CSA) in
the contralesional than ipsilesional limb based on computer tomography images (Odajima, et al.,
1987), but another found no differences in TA volume determined by MRI (Ramsay, et al.,
2011). At the fiber level, Scelsi and coworkers (1984) reported progressively smaller type II
fiber diameter in the contralesional TA with increased time (1-17 months) since stroke, but
Jakobsson et al., (1991) found that fiber CSA was not different between chronic stroke subjects
and healthy controls.
“Neural and Muscular Determinants of Dorsiflexor Weakness in Chronic Stroke Survivors”
by Klein CS, Power GA, Brooks D, Rice CL
Motor Control
© 2013 Human Kinetics, Inc.
Although central neural activation, muscle size, and maximal muscle force generating
capacity are primary determinants of voluntary strength, all three determinants have not been
assessed concurrently in the same stroke subjects; and thus the purpose of this study. More
specifically, we addressed whether weakness arises solely from neural impairments or also
results from atrophy and reduced maximal force generating capacity. In addition to this
comprehensive assessment of the determinants of weakness, the findings should provide some
insight into the conflicting results noted above pertaining to dorsiflexor (TA) size and force
generating capacity. We hypothesized that most of the contralesional dorsiflexor weakness
would reflect reduced activation, but that intrinsic changes in muscle properties also would
contribute in some cases.
METHODS
Participants
Five men and two women (56.9 ± 9.0 years, mean±SD) who had a stroke at least 2 years
before the study were recruited (Table 1). These individuals participated in a previous study of
plantar flexion weakness (Klein, et al., 2010), and showed significant limb differences in
strength, activation, and muscle volume. Therefore the same subjects were tested in the present
study providing a sufficient sample size for these comparisons. Motor impairment of the leg
and foot (Gowland et al., 1993) ranged from mild to moderate (Table 1). Three subjects (no. 4-6)
walked with a more pronounced reduction in knee flexion than the others. Two subjects (no. 4
and 7) used a single point cane when walking, and two others (no. 3 and 6) wore an ankle
orthotic. All participants could walk without assistance, but their gait speed varied threefold, and
the average speed (0.83±0.33 m/s) was about 30% slower than healthy adults (Klein, et al., 2010).
Four subjects (subjects 1, 3, 5, and 6) engaged in 20-30 min of aerobic exercise about two times
“Neural and Muscular Determinants of Dorsiflexor Weakness in Chronic Stroke Survivors”
by Klein CS, Power GA, Brooks D, Rice CL
Motor Control
© 2013 Human Kinetics, Inc.
per week at a fitness club over the previous year. We also determined bilateral MVC and evoked
torque in 7 men with no history of neurological impairment (38±16 years, range, 24-69;
175.2±14.7 cm; 82±13 kg). Informed written and verbal consent were obtained in all subjects
and the study was approved by the local research ethics committees of our institution.
Experimental set-up
Only one leg was assessed during each of the two visits to the laboratory in order to
minimize general fatigue of the participants. The testing order of the contralesional and
ipsilesional limb, and right-left side of the controls, was randomized. Subjects were seated with
their leg positioned in a custom torque measuring device (Klein, et al., 2010). The knee and hip
joints were flexed to 90°, and a clamp stabilized the knee from above. The foot rested on a plate
and was secured with straps across the instep and proximal to the great toe. The ankle was
plantar flexed 30° from the neutral (0°) position. At this angle, the peronei are shortened and are
therefore less effective in counteracting the evoked torque of the dorsiflexors. Also, 30° is near
optimal for MVC torque (Marsh, Sale, McComas, & Quinlan, 1981) and optimal for 50 Hz
torque (van Schaik, Hicks, & McCartney, 1994).
The compound muscle action potential (M-wave) and MVC EMG were recorded with
disposable silver-silver chloride disc electrodes positioned in a bipolar configuration (Bortec
Biomedical Ltd., Calgary, Alberta). The recording electrodes were placed over the distal third of
lateral gastrocnemius (LG) medial gastrocnemius (MG), and midline of the soleus (2 cm below
the distal end of the MG) using a 2 cm center-to-center spacing. For the TA, the distal electrode
was placed at the border of the muscle belly and tendon, and the other electrode was placed 4-5
cm proximally.
“Neural and Muscular Determinants of Dorsiflexor Weakness in Chronic Stroke Survivors”
by Klein CS, Power GA, Brooks D, Rice CL
Motor Control
© 2013 Human Kinetics, Inc.
The EMG was amplified (x 500) and filtered between 30 Hz and 1 kHz (Astro-Medical,
Model P511, West Warwick, RI, USA). Torque was sensed by a transducer beneath the ankle
joint (LCDA-500, Omega Engineering Inc, Stamford, CT, USA), and amplified (x 400) and
filtered (DC-100 Hz). The EMG and torque signals were digitally converted by a 12-bit
converter (1401 Plus, Cambridge Electronic Design, Cambridge, UK) at sampling rates of 2000
Hz and 500 Hz, respectively, and analyzed with Spike 2 software (Spike 2, version 7.03,
Cambridge Electronic Design).
In order to find the optimal site for stimulation of the common fibular nerve, a bar
electrode (1 cm diameter discs, 3 cm spacing; Medtronic, Skovlunde, Denmark) was placed
immediately inferior to the fibular head and manually adjusted until M-waves were evoked
during submaximal stimuli. For all subsequent recordings, 3 cm diameter round carbon rubber
electrodes (Empi, St. Paul, Minnesota, USA), coated in conductive gel, were positioned at the
optimal site and secured with tape. These electrodes minimized subject discomfort during 50 Hz
stimulation.
Protocol. Single pulses (50 µs) of progressively greater current intensity (5 mA
increments) were applied by a constant current stimulator ( Model DS7AH, Digitimer) every 5 s
until the TA M-wave peak-to-peak amplitude did not increase further (ie., Mmax). Subjects
generated a few practice voluntary contractions of the dorsiflexors at ~ 50% effort. Three to four
MVCs, each lasting about 4-5 s followed by a two min rest, were recorded. Strong
encouragement was provided during the MVC and a display of the on-going torque trace was
provided. Before and after each MVC, single supramaximal (120 % of Mmax current) pulses
were applied so that percentage activation could be determined (Belanger & McComas, 1981).
“Neural and Muscular Determinants of Dorsiflexor Weakness in Chronic Stroke Survivors”
by Klein CS, Power GA, Brooks D, Rice CL
Motor Control
© 2013 Human Kinetics, Inc.
The stimuli were triggered manually by the investigator about 2-4 s after the beginning of the
MVC, when there was a plateau in the torque trace, and also about 1 s after the MVC finished.
Three minutes after recording the MVCs, two practice 50 Hz contractions (each 0.5 s)
were evoked at progressively greater submaximal current intensities. A 50 Hz train (0.5 s) was
then evoked using the supramaximal current. Supramaximal stimulation of the dorsiflexors at 50
Hz is well tolerated and the evoked response reflects the maximal torque that can be generated
by the dorsiflexor muscles (independent of subject volition) (Marsh, et al., 1981). Inclusion of
this measure together with the assessment of muscle volume allowed us to determine whether
changes in muscle properties contribute to the loss of MVC strength. Specifically, smaller
contralesional than ipsilesional 50 Hz torque would indicate a loss in torque generating capacity,
either because of atrophy or reduced specific tension (force per unit area) of the muscle fibers, or
both. Specific torque (50 Hz torque/muscle volume) was calculated in the present study as an
indirect measure of specific tension. After recording the 50 Hz torque, subjects completed three
to four plantar flexor MVCs, each lasting 4-5 s.
MRI. The participants were placed in a supine position in a 3T whole body scanner with
the shank in a quad head coil (Signa Excite HDx, General Electric Company). The knee was
extended, the leg supported with padding, and the ankle was stabilized in ~20 ° of plantar flexion.
Images were acquired from each leg separately using serial T1-weighted spin-echo sequences.
Initially, scout images of the leg were acquired in the coronal and sagittal planes. After the scout
images, about 40-50 axial slices was aligned perpendicular to the tibial shaft in the coronal and
sagittal planes between the knee and ankle joints. The axial images were acquired in an
interleaved manner using the following parameters; echo time 18 ms, repetition time 850 ms,
matrix 256 x 256, field of view 200 mm, slice thickness 10 mm, interslice gap 0 mm, number of
“Neural and Muscular Determinants of Dorsiflexor Weakness in Chronic Stroke Survivors”
by Klein CS, Power GA, Brooks D, Rice CL
Motor Control
© 2013 Human Kinetics, Inc.
acquisitions 2. Our results in the stroke subjects were compared with the ample age-matched
control data reported for this muscle group from our lab (McNeil, Vandervoort, & Rice, 2007)
and others (Kent-Braun & Ng, 1999).
Data analysis
MVC. The peak MVC torque was determined for each trial. The TA root-mean-square
EMG over a 500 ms period was determined just prior to the interpolated twitch, and was
normalized to the Mmax (ie. RMS EMG/peak-to-peak amplitude of the M-wave). The
interpolated torque was equal to the torque at the onset of the stimulus minus the evoked peak
torque. Activation percentage was equal to the following: [1- (Ts/Tr)] x 100 %, where Ts was the
interpolated torque evoked by the stimulus during the MVC, and Tr was the torque of twitch after
the MVC.
Antagonist coactivation percentage. The root-mean-square EMG of the soleus, LG, and
MG over 500 ms of the dorsiflexor MVC was expressed as a percentage of the muscle’s
maximum EMG recorded during the plantar flexor MVC.
Dorsiflexor volume. The MR images were converted to TIFF files from their original
DICOM format. All images were analyzed by one investigator using available software (ImageJ,
ver 1.38, National Institutes of Health, Bethesda, MD). The border of the dorsiflexor muscle
group that included the tibialis anterior, extensor hallucis longus, extensor digitorum longus, and
peroneus tertius, was manually traced for all axial slices from muscle origin to insertion and the
corresponding CSAs determined. Intramuscular fat in each image was subtracted from the
muscle CSA with a user-defined threshold. Dorsiflexor volume was calculated as the sum of fat-
free CSA area times slice thickness for all slices of the muscle group. Specific torque was
calculated as maximal 50 Hz torque divided by dorsiflexor volume.
“Neural and Muscular Determinants of Dorsiflexor Weakness in Chronic Stroke Survivors”
by Klein CS, Power GA, Brooks D, Rice CL
Motor Control
© 2013 Human Kinetics, Inc.
Statistics. Paired and unpaired t-tests were used to compare side-to-side differences
within a group and between groups, respectively, for all measures except voluntary activation
percentage, for which the Mann-Whitney U-test was used. The relationship between measures
was determined with Pearson’s product-moment correlation coefficients. Data are presented as
means±SD, and differences were considered significant when P<0.05.
RESULTS
MVC torque. Representative MVC recordings in two stroke subjects are shown in Fig. 1.
In one, peak MVC torque was similar in both legs, although contralesional torque declined
slightly toward the end of the contraction (Fig. 1A, uppermost two traces). Also, there was no
obvious interpolated twitch in either leg. In the other subject, peak contralesional MVC torque
was 30% of the ipsilesional side (Fig.1B). Reduced contralesional activation was apparent,
shown by the interpolated twitch and sparse TA EMG. In six of the seven subjects, the MVC
torque was less in the contralesional than ipsilesional limb, and the mean values were different
(P =0.04, Fig. 2, Table 2).
MVC EMG amplitude and activation percentage. The TA Mmax was not significantly
different between the contralesional and ipsilesional limb (P =0.70, Table 2). The MVC root-
mean-square EMG, normalized to the Mmax, was less in the contralesional than ipsilesional limb
in all subjects, and the mean values were different (P =0.01, Fig. 2, Table 2). Activation
percentage via twitch interpolation was less in in the contralesional than ipsilesional limb, but the
mean values were not different (P =0.2, Table 2). Those with greater weakness tended to have
larger activation deficits. Hence, relative contralesional MVC (% ipsilesional side) was
associated with relative EMG (r2=0.71, P=0.01) and activation percentage (r
2=0.77, P=0.01).
Because subject 7 could not generate any voluntary dorsiflexor torque, a value of zero was
“Neural and Muscular Determinants of Dorsiflexor Weakness in Chronic Stroke Survivors”
by Klein CS, Power GA, Brooks D, Rice CL
Motor Control
© 2013 Human Kinetics, Inc.
assigned for each of his contralesional MVC torque, EMG amplitude, and activation scores and
these zero values were included in the means presented in table 2. The reported statistically
significant differences between the contralesional and ipsilesional means for MVC torque, EMG
amplitude, and percent activation were unchanged when data were reanalyzed with subject 7
excluded (N=6); 34.8±18.3 vs. 43.3±13 vs. Nm (P <0.05), 0.050±0.022 vs. 0.120±0.046 (P
<0.05), and 91.1±17.2 vs. 98.9±1.0 (P= 0.30), respectively.
Antagonist coactivation percentage. The mean antagonist EMG amplitude (mV) was
less in the contralesional than the ipsilesional leg in the soleus (0.015±0.005 vs. 0.27±0.004,
P=0.03) and gastrocnemii (0.013±0.012 vs. 0.023±0.016, P=0.005). The soleus coactivation
percentages ranged from 10.6%-110.7% and 11.4%-21.7% in the contralesional and ipsilesional
limb, respectively. The corresponding values for the gastrocnemii were 6.8%-70.3% and 4.3%-
26.4%. The mean soleus and gastrocnemii coactivation percentages were larger in the
contralesional than ipsilesional limb, but the differences were not significant (P= 0.2, Table 2).
The larger contralesional means were mainly due to the values recorded in subject 6 (110% and
70% in the soleus and gastrocnemii, respectively). The augmented coactivation percentage in this
subject reflected a larger absolute EMG coactivation (mV) in the gastrocnemii, but not the soleus,
combined with a dramatically smaller absolute MVC EMG of both muscles; 12% and 5% of the
ipsilesional side, respectively. Similar to the findings of others (Clark, et al., 2006; Lum, et al.,
2004; Newham & Hsiao, 2001; Wagner, et al., 2007), our results reveal little evidence of
excessive coactivation in the contralesional limb.
50 Hz torque, muscle volume, and specific torque. The 50 Hz torque recordings of two
subjects are shown in Fig 3 and demonstrate that the evoked torques were similar between sides.
In all subjects except one (no. 4), contralesional 50Hz torque was equal to or larger than the
“Neural and Muscular Determinants of Dorsiflexor Weakness in Chronic Stroke Survivors”
by Klein CS, Power GA, Brooks D, Rice CL
Motor Control
© 2013 Human Kinetics, Inc.
ipsilesional value, and the means were not different (P =0.3, Table 2). The lack of a difference in
mean 50 Hz torque generating capacity between limbs supports the findings of a previous study
(Landau & Sahrmann, 2002), but, unlike their large side-to-side 50 Hz differences in individual
subjects (up to 150%), differences in the present subjects were ≤ 25% (see discussion). The total
dorsiflexor volume (cm3), fat volume (cm
3), and percentage of total volume that was fat, was not
significantly different between the contralesional and ipsilesional limbs; 264.8±69.0, 4.6±2.3,
1.9±1.1% vs 255.5±81.2, 5.6±2.5, 2.5±1.7% (P=0.4, P=0.2, P=0.1, respectively). Contralesional
fat-free volume (and CSA) was similar to or larger than ipsilesional volume across subjects (Fig.
2), and the means were not different (P =0.4, Table 2). The differences in the 50 Hz
torque/volume ratio between limbs were not different (P =0.9, Table 2).
Comparisons to control subjects. The MVC torque (P=0.04) and MVC EMG (P=0.003)
were significantly less in the contralesional limb compared to the right limb of the 7 controls, but
TA Mmax, activation, coactivation, and 50 Hz torque did not differ significantly (Table 2). There
were no significant differences between ipsilesional and control means for any parameter (Table
2). Right-left differences in mean TA Mmax, control MVC torque, MVC EMG, and 50 Hz
torque were modest (<16%) and not significant (P >0.05).
DISCUSSION
In this study, we assessed both central and peripheral determinants of weakness in
chronic stroke subjects. Our findings indicate that most of the weakness reflects a reduction in
central neural drive to the motoneuron pool, with little contribution from antagonist muscle
activity. The idea among some clinicians that atrophy is commonplace after stroke is not
supported by the present results.
“Neural and Muscular Determinants of Dorsiflexor Weakness in Chronic Stroke Survivors”
by Klein CS, Power GA, Brooks D, Rice CL
Motor Control
© 2013 Human Kinetics, Inc.
Because muscles receive some of their innervation from the ipsilateral motor cortex, the
ipsilesional side may show impairments in activation and weakness following stroke (Adams, et
al., 1990; Newham & Hsiao, 2001). However, in the present study, MVC and 50 Hz torques did
not differ between the ipsilesional and control limbs (Table 2). Although the controls were
younger on average than the stroke subjects, previous work showed little age-related differences
in dorsiflexor properties between 30 and 70 y of age. Hence, mean ipsilesional MVC, 50 Hz
torque, and dorsiflexor CSA of the five men with stroke (47 Nm, 34 Nm, and 14.2 cm2) are
similar to the means reported for older (65 y) healthy men (44 Nm, 30 Nm and 14.3 cm2, 65y)
(Kent-Braun & Ng, 1999; McNeil, et al., 2007; van Schaik, et al., 1994). The preserved
ipsilesional dorsiflexor motor function may reflect overuse of this limb to compensate for
contralesional impairments (Olney, Griffin, Monga, & McBride, 1991).
Contralesional weakness was evident in six of the seven subjects and was associated with
deficits in EMG amplitude and activation percentage. The recorded weakness, particularly
evident in subjects 4, 6, and 7, may be partially attributed to a diminished capacity to recruit and
fully activate the dorsiflexor motoneuron pool. Indeed, one study of stroke subjects found that
the motor unit firing rates of the contralesional TA did not rise above 15 Hz during an MVC
(Frontera, et al., 1997). This level of motor unit firing is less than half of the normal rate and
would be expected to generate smaller peak forces. Others have reported contralesional
dorsiflexor weakness (Adams, et al., 1990; Eng, Lomaglio, & Macintyre, 2009; Landau &
Sahrmann, 2002) and reduced EMG amplitude (Frontera, et al., 1997; Jakobsson, et al., 1991;
Knorr, et al., 2011), but the contribution of changes in whole muscle morphology was not
evaluated.
“Neural and Muscular Determinants of Dorsiflexor Weakness in Chronic Stroke Survivors”
by Klein CS, Power GA, Brooks D, Rice CL
Motor Control
© 2013 Human Kinetics, Inc.
Our results indicate that reduced central neural drive is the primary determinant of
contralesional dorsiflexor weakness in these subjects because of a lack of atrophy or any
contractile impairment combined with their deficits in activation and EMG amplitude. However,
the percent contribution of reduced neural drive to weakness may be underestimated when based
on twitch interpolation data and overestimated when based on the EMG amplitude results (Fig.
2) (Klein, et al., 2010). Although twitch interpolation is considered to be one of the better
methods to assess voluntary activation, it is not without limitations. The sensitivity of the
method, or the ability to detect small deficits in dorsiflexor activation, is reduced at higher (> 80
% MVC) torques, possibly because the fibular (peroneal) muscles can act as antagonists when
activated during electrical stimulation (Belanger & McComas, 1981). In healthy adults, the
relationship between relative (%MVC) EMG amplitude and dorsiflexor torque is curvilinear
(Garland, Garner, & McComas, 1988). Hence, at a contraction strength equal to 50% MVC
torque, the corresponding EMG is 30% of the MVC EMG. This difference between relative
EMG and relative torque may widen after stroke because of a reduction in maximal motor unit
firing rate in the contralesional limb (Frontera, et al., 1997), and could explain the relatively
larger deficits in contralesional EMG than MVC torque (Fig. 2).
Dorsiflexor atrophy was not evident in the present subjects and supports the concept of
little to no loss in dorsiflexor mass after stroke. Our results confirm previous studies of chronic
stroke subjects that found no evidence of TA atrophy based on the determination of muscle
volume derived from magnetic resonance images (Ramsay, et al., 2011) and fiber area of
biopsies (Jakobsson, et al., 1991). In one study, dorsiflexor CSA, derived from computer
tomography images, was about 12% smaller in the contralesional than the ipsilesional limb
(Odajima, et al., 1987). Another reported evidence of contralesional TA fiber atrophy in some
“Neural and Muscular Determinants of Dorsiflexor Weakness in Chronic Stroke Survivors”
by Klein CS, Power GA, Brooks D, Rice CL
Motor Control
© 2013 Human Kinetics, Inc.
stroke subjects, but they may have been less mobile than the present stroke subjects since they
were to undergo corrective foot surgery (split anterior tibial tendon transfer) to improve
ambulation (Slager, et al., 1985).
The lack of atrophy and contractile impairment in the present subjects is evident despite
deficits in EMG and activation (ie. no. 4 and 7). Subject 7 was unable to generate any EMG or
torque during the MVC, and his TA activity during gait was also found to be negligible.
Immediately after the torque recordings of the contralesional and ipsilesional limbs, we had
subject 7 walk back and forth a distance of 5 m in the laboratory at his preferred speed while
recording the associated EMG activity using the same electrodes (data not shown). During this 5
m walk, his contralesional mean TA EMG amplitude at heel strike was found to be about 5% of
the ipsilesional TA MVC EMG amplitude; much less than typically recorded in healthy controls
(Jakobsson, et al., 1991). Our whole muscle results support and extend the findings of a previous
study in which there was no significant contralesional TA fiber atrophy, even though the TA
EMG amplitude during walking was less than 10% of adult controls (Jakobsson, et al., 1991).
Together, these observations suggest that recruitment of a large portion of the dorsiflexors is not
a necessary precondition for maintenance of muscle mass and force generating capacity
following stroke. Rather, factors independent of muscle activation, including passive mechanical
tension or neurotrophic support may play important roles (McComas, Sica, Upton, & Aguilera,
1973; Yucesoy & Huijing, 2007).
In subject 6, hypertrophy was apparent in the contralesional dorsiflexors (+28%) and the
peronei (+42%) but with atrophy of the gastrocnemii (-50%) (Klein, et al., 2010), indicating that
responses may be muscle-dependent in some cases (Odajima, et al., 1987; Ploutz-Snyder, Clark,
Logan &Turk 2006; Prado-Medeiros et al., 2012). Scattered fiber hypertrophy has been noted in
“Neural and Muscular Determinants of Dorsiflexor Weakness in Chronic Stroke Survivors”
by Klein CS, Power GA, Brooks D, Rice CL
Motor Control
© 2013 Human Kinetics, Inc.
the TA and other muscles after stroke (Jakobsson, et al., 1991; Slager, et al., 1985). Interesting,
in some individuals with anterior cruciate ligament injury, TA volume was also unexpectedly
larger in the injured limb compared to the non-injured limb (Binder-Macleod & Buchanan, 2006).
Like these types of injuries, peculiar changes in gait mechanics following stroke (Perry, Waters,
& Perrin, 1978) may lead to stretch-induced hypertrophy of some muscles and disuse atrophy of
others. In subject 6, the equinovarus foot position during gait may have resulted in stretch-
induced hypertrophy of the TA and peronei.
We explored intrinsic contractile function by comparing side-to-side 50 Hz torque
differences using maximal stimulation of the common fibular nerve and which could be related
to muscle quantity. In one previous study of chronic stroke, contralesional 50Hz torque, tested
by using pad stimulation over only the TA, was found to differ widely (~20% to 150% of the
ipsilesional value in one-half of the subjects), which was not easy to explain (Landau &
Sahrmann, 2002). Compared to their data (Landau & Sahrmann, 2002) we found that the side-to-
side 50 Hz torque differences were more modest in the stroke subjects (≤ 25%) and controls (≤
9%). The design to isolate the current field to the TA in the prior study (Landau & Sahrmann,
2002) may not have accounted for variable activation spread to other local dorsiflexors and
plantar flexors (peronei). Supramaxmial nerve stimulation, as applied in the present study, is
likely a more precise method for assessing limb differences in torque generating capacity
because all dorsiflexor and peronei muscles are maximally activated.
Study limitations. With a limited sample size and inclusion of only persons with chronic
neurological impairments who are mobile and physically active, these findings are not
necessarily representative of the wider stroke population. Dorsiflexor atrophy and weakness
would be expected to be greater in those who are less mobile and inactive (Eng, et al., 2009;
“Neural and Muscular Determinants of Dorsiflexor Weakness in Chronic Stroke Survivors”
by Klein CS, Power GA, Brooks D, Rice CL
Motor Control
© 2013 Human Kinetics, Inc.
Odajima, et al., 1987). In addition, weakness and antagonist coactivation may be more
pronounced when measured during dynamic contractions as opposed to isometric conditions
employed here (Lum, et al., 2004).
Conclusions. Despite weakness and reduced EMG amplitude, muscle volume, 50 Hz
torque, and specific torque were well preserved in the stroke subjects. Our results suggest that
much of the weakness can be attributed to a loss of central neural drive to the agonist
motoneuron pool. The preservation of contralesional dorsiflexor muscle properties may be
explained in part by their relatively preserved mobility and regular physical activity.
Acknowledgements
The authors thank the subjects who volunteered for this study and the Medical Imaging staff at
Toronto Western Hospital for their technical support. This research was supported by the Dean’s
Fund, Faculty of Medicine, University of Toronto.
“Neural and Muscular Determinants of Dorsiflexor Weakness in Chronic Stroke Survivors”
by Klein CS, Power GA, Brooks D, Rice CL
Motor Control
© 2013 Human Kinetics, Inc.
References
Adams, R. W., Gandevia, S. C., & Skuse, N. F. (1990). The distribution of muscle weakness in
upper motoneuron lesions affecting the lower limb. Brain, 113 ( Pt 5), 1459-1476.
http://www.ncbi.nlm.nih.gov/pubmed/2245306
Arene, N., & Hidler, J. (2009). Understanding motor impairment in the paretic lower limb after a
stroke: a review of the literature. Top Stroke Rehabil, 16(5), 346-356.
http://www.ncbi.nlm.nih.gov/pubmed/19903653
Belanger, A. Y., & McComas, A. J. (1981). Extent of motor unit activation during effort. J Appl
Physiol, 51(5), 1131-1135. http://www.ncbi.nlm.nih.gov/pubmed/7298453
Binder-Macleod, B. I., & Buchanan, T. S. (2006). Tibialis anterior volumes and areas in ACL-
injured limbs compared with unimpaired. Med Sci Sports Exerc, 38(9), 1553-1557.
http://www.ncbi.nlm.nih.gov/pubmed/16960514
Clark, D. J., Condliffe, E. G., & Patten, C. (2006). Activation impairment alters muscle torque-
velocity in the knee extensors of persons with post-stroke hemiparesis. Clin Neurophysiol,
117(10), 2328-2337. http://www.ncbi.nlm.nih.gov/pubmed/16926111
Dubo, H. I., Peat, M., Winter, D. A., Quanbury, A. O., Hobson, D. A., Steinke, T., & Reimer, G.
(1976). Electromyographic temporal analysis of gait: normal human locomotion. Arch
Phys Med Rehabil, 57(9), 415-420. http://www.ncbi.nlm.nih.gov/pubmed/962568
Eng, J. J., Lomaglio, M. J., & Macintyre, D. L. (2009). Muscle torque preservation and physical
activity in individuals with stroke. Med Sci Sports Exerc, 41(7), 1353-1360.
http://www.ncbi.nlm.nih.gov/pubmed/19516167
“Neural and Muscular Determinants of Dorsiflexor Weakness in Chronic Stroke Survivors”
by Klein CS, Power GA, Brooks D, Rice CL
Motor Control
© 2013 Human Kinetics, Inc.
Frontera, W. R., Grimby, L., & Larsson, L. (1997). Firing rate of the lower motoneuron and
contractile properties of its muscle fibers after upper motoneuron lesion in man. Muscle
Nerve, 20(8), 938-947. http://www.ncbi.nlm.nih.gov/pubmed/9236783
Garland, S. J., Garner, S. H., & McComas, A. J. (1988). Reduced voluntary electromyographic
activity after fatiguing stimulation of human muscle. J Physiol, 401, 547-556.
http://www.ncbi.nlm.nih.gov/pubmed/3171996
Gowland, C., Stratford, P., Ward, M., Moreland, J., Torresin, W., Van Hullenaar, S., . . . Plews,
N. (1993). Measuring physical impairment and disability with the Chedoke-McMaster
Stroke Assessment. Stroke, 24(1), 58-63. http://www.ncbi.nlm.nih.gov/pubmed/8418551
Horstman, A. M., Beltman, M. J., Gerrits, K. H., Koppe, P., Janssen, T. W., Elich, P., & de Haan,
A. (2008). Intrinsic muscle strength and voluntary activation of both lower limbs and
functional performance after stroke. Clin Physiol Funct Imaging, 28(4), 251-261.
http://www.ncbi.nlm.nih.gov/pubmed/18355344
Jakobsson, F., Edstrom, L., Grimby, L., & Thornell, L. E. (1991). Disuse of anterior tibial
muscle during locomotion and increased proportion of type II fibres in hemiplegia. J
Neurol Sci, 105(1), 49-56. http://www.ncbi.nlm.nih.gov/pubmed/1795169
Kent-Braun, J. A., & Ng, A. V. (1999). Specific strength and voluntary muscle activation in
young and elderly women and men. J Appl Physiol, 87(1), 22-29.
http://www.ncbi.nlm.nih.gov/pubmed/10409554
Klein, C. S., Brooks, D., Richardson, D., McIlroy, W. E., & Bayley, M. T. (2010). Voluntary
activation failure contributes more to plantar flexor weakness than antagonist
coactivation and muscle atrophy in chronic stroke survivors. J Appl Physiol, 109(5),
1337-1346. http://www.ncbi.nlm.nih.gov/pubmed/20724561
“Neural and Muscular Determinants of Dorsiflexor Weakness in Chronic Stroke Survivors”
by Klein CS, Power GA, Brooks D, Rice CL
Motor Control
© 2013 Human Kinetics, Inc.
Knorr, S., Ivanova, T. D., Doherty, T. J., Campbell, J. A., & Garland, S. J. (2011). The origins of
neuromuscular fatigue post-stroke. Exp Brain Res, 214(2), 303-315.
http://www.ncbi.nlm.nih.gov/pubmed/21847644
Knutsson, E., & Richards, C. (1979). Different types of disturbed motor control in gait of
hemiparetic patients. Brain, 102(2), 405-430.
http://www.ncbi.nlm.nih.gov/pubmed/455047
Landau, W. M., & Sahrmann, S. A. (2002). Preservation of directly stimulated muscle strength in
hemiplegia due to stroke. Arch Neurol, 59(9), 1453-1457.
http://www.ncbi.nlm.nih.gov/pubmed/12223033
Levin, M. F., & Hui-Chan, C. (1994). Ankle spasticity is inversely correlated with antagonist
voluntary contraction in hemiparetic subjects. Electromyogr Clin Neurophysiol, 34(7),
415-425. http://www.ncbi.nlm.nih.gov/pubmed/7859670
Lum, P. S., Patten, C., Kothari, D., & Yap, R. (2004). Effects of velocity on maximal torque
production in poststroke hemiparesis. Muscle Nerve, 30(6), 732-742.
http://www.ncbi.nlm.nih.gov/pubmed/15468340
Marsh, E., Sale, D., McComas, A. J., & Quinlan, J. (1981). Influence of joint position on ankle
dorsiflexion in humans. J Appl Physiol, 51(1), 160-167.
http://www.ncbi.nlm.nih.gov/pubmed/7263411
McComas, A. J., Sica, R. E., Upton, A. R., & Aguilera, N. (1973). Functional changes in
motoneurones of hemiparetic patients. J Neurol Neurosurg Psychiatry, 36(2), 183-193.
http://www.ncbi.nlm.nih.gov/pubmed/4350702
“Neural and Muscular Determinants of Dorsiflexor Weakness in Chronic Stroke Survivors”
by Klein CS, Power GA, Brooks D, Rice CL
Motor Control
© 2013 Human Kinetics, Inc.
McNeil, C. J., Vandervoort, A. A., & Rice, C. L. (2007). Peripheral impairments cause a
progressive age-related loss of strength and velocity-dependent power in the dorsiflexors.
J Appl Physiol, 102(5), 1962-1968. http://www.ncbi.nlm.nih.gov/pubmed/17303705
Newham, D. J., & Hsiao, S. F. (2001). Knee muscle isometric strength, voluntary activation and
antagonist co-contraction in the first six months after stroke. Disabil Rehabil, 23(9), 379-
386. http://www.ncbi.nlm.nih.gov/pubmed/11394588
Odajima, N., Ishiai, S., Okiyama, R., Furukawa, T., & Tsukagoshi, H. (1987). [CT findings of
leg muscles in the hemiplegics due to cerebrovascular accidents--correlation to disuse
atrophy]. Rinsho Shinkeigaku, 27(9), 1154-1162.
http://www.ncbi.nlm.nih.gov/pubmed/3440361
Olney, S. J., Griffin, M. P., Monga, T. N., & McBride, I. D. (1991). Work and power in gait of
stroke patients. Arch Phys Med Rehabil, 72(5), 309-314.
http://www.ncbi.nlm.nih.gov/pubmed/2009047
Perry, J., Waters, R. L., & Perrin, T. (1978). Electromyographic analysis of equinovarus
following stroke. Clin Orthop Relat Res(131), 47-53.
http://www.ncbi.nlm.nih.gov/pubmed/657644
Ploutz-Snyder, L. L., Clark, B. C., Logan, L., & Turk, M. (2006). Evaluation of spastic muscle in
stroke survivors using magnetic resonance imaging and resistance to passive motion.
Arch Phys Med Rehabil, 87(12), 1636-1642.
http://www.ncbi.nlm.nih.gov/pubmed/17141645
Prado-Medeiros, C. L., Silva, M. P., Lessi, G. C., Alves, M. Z., Tannus, A., Lindquist, A. R., &
Salvini, T. F. (2012). Muscle atrophy and functional deficits of knee extensors and
“Neural and Muscular Determinants of Dorsiflexor Weakness in Chronic Stroke Survivors”
by Klein CS, Power GA, Brooks D, Rice CL
Motor Control
© 2013 Human Kinetics, Inc.
flexors in people with chronic stroke. Phys Ther, 92(3), 429-439.
http://www.ncbi.nlm.nih.gov/pubmed/22135704
Ramsay, J. W., Barrance, P. J., Buchanan, T. S., & Higginson, J. S. (2011). Paretic muscle
atrophy and non-contractile tissue content in individual muscles of the post-stroke lower
extremity. J Biomech, 44(16), 2741-2746.
http://www.ncbi.nlm.nih.gov/pubmed/21945568
Scelsi, R., Lotta, S., Lommi, G., Poggi, P., & Marchetti, C. (1984). Hemiplegic atrophy.
Morphological findings in the anterior tibial muscle of patients with cerebral vascular
accidents. Acta Neuropathol, 62(4), 324-331.
http://www.ncbi.nlm.nih.gov/pubmed/6730908
Slager, U. T., Hsu, J. D., & Jordan, C. (1985). Histochemical and morphometric changes in
muscles of stroke patients. Clin Orthop Relat Res(199), 159-168.
http://www.ncbi.nlm.nih.gov/pubmed/4042473
van Schaik, C. S., Hicks, A. L., & McCartney, N. (1994). An evaluation of the length-tension
relationship in elderly human ankle dorsiflexors. J Gerontol, 49(3), B121-127.
http://www.ncbi.nlm.nih.gov/pubmed/8169329
Wagner, J. M., Dromerick, A. W., Sahrmann, S. A., & Lang, C. E. (2007). Upper extremity
muscle activation during recovery of reaching in subjects with post-stroke hemiparesis.
Clin Neurophysiol, 118(1), 164-176. http://www.ncbi.nlm.nih.gov/pubmed/17097340
Yucesoy, C. A., & Huijing, P. A. (2007). Substantial effects of epimuscular myofascial force
transmission on muscular mechanics have major implications on spastic muscle and
remedial surgery. J Electromyogr Kinesiol, 17(6), 664-679.
http://www.ncbi.nlm.nih.gov/pubmed/17395489
“Neural and Muscular Determinants of Dorsiflexor Weakness in Chronic Stroke Survivors”
by Klein CS, Power GA, Brooks D, Rice CL
Motor Control
© 2013 Human Kinetics, Inc.
Yusevich, Y. S. (1968). The significance of "global" electromyography for analysing the
pathological mechanisms of spastic paralysis. Electromyography, 8(2), 135-157.
http://www.ncbi.nlm.nih.gov/pubmed/5705819
“Neural and Muscular Determinants of Dorsiflexor Weakness in Chronic Stroke Survivors”
by Klein CS, Power GA, Brooks D, Rice CL
Motor Control
© 2013 Human Kinetics, Inc.
Figure 1. Ipsilesional and contralesional dorisflexor MVC torque (uppermost two traces) and
raw EMG of the TA, soleus, LG and MG in two stroke subjects (contralesional EMG is the
lower trace of each pair). (A) In this subject (no. 2), peak MVC torque is similar between sides
(B) In this subject (no. 4), MVC torque was much less in the contralesional than the ipsilesional
limb. Note the interpolated twitch and sparse TA EMG in the contralesional limb.
“Neural and Muscular Determinants of Dorsiflexor Weakness in Chronic Stroke Survivors”
by Klein CS, Power GA, Brooks D, Rice CL
Motor Control
© 2013 Human Kinetics, Inc.
Figure 2. Individual contralesional dorsiflexor voluntary activation (▼), and relative
contralesional values (% ipsilesional side) for MVC torque (●), MVC EMG (▲), 50 Hz torque
(♦), and fat-free muscle volume (■) for subjects 1-7.
“Neural and Muscular Determinants of Dorsiflexor Weakness in Chronic Stroke Survivors”
by Klein CS, Power GA, Brooks D, Rice CL
Motor Control
© 2013 Human Kinetics, Inc.
Figure 3. Evoked dorsiflexor torque and EMG during supramaximal 50 Hz stimulation in
subject 2 (A) and subject 7 (B). For each subject, the torque and EMG are shown for the
contralesional limb (dotted line and lower EMG trace) and ipsilesional limb (continuous line and
upper EMG trace).
“Neural and Muscular Determinants of Dorsiflexor Weakness in Chronic Stroke Survivors”
by Klein CS, Power GA, Brooks D, Rice CL
Motor Control
© 2013 Human Kinetics, Inc.
Table 1. Characteristics of the stroke subjects
Subject
no.
Sex Age
(yr)
Ht
(cm)
Wt
(kg)
CMSA
Leg/foot
Speed
(m/s)
TSO
(months)
1
M 67 185.4 104.5 5/5 1.35 36
2 M 63 180.3 81.8 4/4 1.0 43
3 F 61 162.6 61.4 4/3 0.63 37
4 M 56 177.8 68.2 4/3 0.49 27
5 M 51 185.3 95.4 3/3 0.58 24
6 F 40 167.6 68.2 3/3 0.82 51
7 M 60 178.0 61.4 4/2 0.91 48
Abbreviations: M, male; F, female; Ht, height, Wt, weight; CMSA, Chedoke-McMaster Stroke
Assessment Score; Speed, walking speed; TSO, time since onset of stroke
“Neural and Muscular Determinants of Dorsiflexor Weakness in Chronic Stroke Survivors”
by Klein CS, Power GA, Brooks D, Rice CL
Motor Control
© 2013 Human Kinetics, Inc.
Table 2. Dorsiflexor properties in stroke and control subjects
Measure
Contralesional Ipsilesional Control
TA Mmax (mV)
7.8 ± 1.2 8.0 ± 2.8 7.4 ± 2.6
MVC (Nm)
29.8 ± 21.3* 42.5 ± 12.0 49.7 ± 7.1
MVC EMG
0.043 ± 0.028* 0.118 ± 0.045 0.09 ± 0.01
MVC activation (%)
78.1 ± 37.8 98.7 ± 1.0 98.2 ± 1.5
Soleus coactivation (%)
35.4 ± 37.6 16.3 ± 3.9 19.1 ± 13.2
Gastrocnemii coactivation (%) 25.8 ± 26.6 10.1 ± 8.1 18.0 ± 6.1
50 Hz torque (Nm)
32.3 ± 12.6 30.4 ± 10.5 35.7 ± 6.6
Dorsiflexor volume (cm3)
260 ± 69 250 ± 82 _
Dorsiflexor CSA (cm2)
13.2±3.0 12.9 ±4.1 _
50Hz/volume (Nm/cm3)
0.12 ± 0.03 0.12 ± 0.02 _
Note the MVC EMG values were normalized to the TA Mmax.
* Significantly different compared to the ipsilesional limb and control limb.