Isometric Contractions to Is Specifically Modulated in Lengthening

Excitability at the Motoneuron Pool and Motor Cortex
Is Specifically Modulated in Lengthening Compared to
Isometric Contractions
M. Gruber, V. Linnamo, V. Strojnik, T. Rantalainen and J. Avela
J Neurophysiol 101:2030-2040, 2009. First published 4 February 2009; doi:10.1152/jn.91104.2008
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Specific modulation of corticospinal and spinal excitabilities during maximal voluntary
isometric, shortening and lengthening contractions in synergist muscles
Julien Duclay, Benjamin Pasquet, Alain Martin and Jacques Duchateau
J Physiol, June 1, 2011; 589 (11): 2901-2916.
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J Neurophysiol 101: 2030 –2040, 2009.
First published January 28, 2008; doi:10.1152/jn.91104.2008.
Excitability at the Motoneuron Pool and Motor Cortex Is Specifically
Modulated in Lengthening Compared to Isometric Contractions
M. Gruber,1-3 V. Linnamo,1 V. Strojnik,4 T. Rantalainen,1,5 and J. Avela1
1
Neuromuscular Research Center, Department of Biology of Physical Activity, University of Jyväskylä, Jyväskylä, Finland;
Institute of Sport and Sport Science, University of Freiburg, Freiburg, Germany; 3Department of Training and Movement Science,
University of Potsdam, Potsdam, Germany; 4Laboratory of Biomechanics, University of Ljubljana, Ljubljana, Slovenia; and 5Department
of Mechanical Engineering, University of Lappeenranta, Lappeenranta, Finland
2
Submitted 3 October 2008; accepted in final form 27 January 2009
According to muscle models, the force during a maximum
lengthening contraction should exceed force during a maximum isometric contraction by ⱕ50% due to short range stiffness (Rack and Westbury 1974). For in vivo experiments,
higher lengthening forces were only observed at the very
beginning of muscle lengthening with preactivated muscles
(Komi et al. 2000; Linnamo et al. 2002, 2003, 2006) but not for
the whole range of motion (Aagaard et al. 2000; Komi et al.
2000; Linnamo et al. 2002, 2003, 2006; Pinniger et al. 2000;
Seger and Thorstensson 2000; Westing et al. 1991). This
inability to reach the maximal potential force level in the later
phase of lengthening has been attributed to a failure of muscle
activation (Babault et al. 2001; Loscher and Nordlund 2002;
Pinniger et al. 2000; Seger and Thorstensson 2000; Webber
and Kriellaars 1997; Westing et al. 1990).
Only a few studies have examined the underlying mechanisms of muscle activation failure during maximum lengthening contractions. Duclay et al. (Duclay and Martin 2005) found
depressed H-reflexes but unchanged V-waves as compared with
isometric and shortening contractions. Loscher and Nordlund
(2002) reported unchanged areas of motor-evoked potentials
(MEP) elicited by transcranial magnetic stimulation (TMS)
when they compared maximal lengthening and shortening
elbow flexions (Loscher and Nordlund 2002). For submaximal
contraction levels, similar findings were presented regarding
the depression of H-reflexes (Abbruzzese et al. 1994; Nordlund
et al. 2002; Romano and Schieppati 1987). However, unlike in
maximal contractions, reduced MEPs were reported for submaximal lengthening compared with shortening contractions
(Abbruzzese et al. 1994; Sekiguchi et al. 2001, 2003). Consequently, it seems appropriate to assume that neural control of
lengthening contractions may be unique (for review, see Enoka
1996).
There is a difference in neural control between submaximal
lengthening contractions, where motor output has to be controlled carefully by the CNS, and maximal lengthening contractions, where maximal voluntary drive is required but could
result in damage to the muscle (Avela et al. 1999; Chen et al.
2003; Crameri et al. 2007; Nosaka et al. 2002). Nevertheless,
for both maximal and submaximal lengthening contractions, it
was hypothesized that a unique control scheme might mainly
act at the spinal level (Aagaard et al. 2000; Abbruzzese et al.
1994; Duclay and Martin 2005; Loscher and Nordlund 2002;
Sekiguchi et al. 2001, 2003). However, because of methodological limitations, these studies could not refer directly to the
site (cortical and/or spinal) of the observed changes. Therefore
the aim of this study was to identify the location of neural
mechanisms (cortical vs. spinal) involved in the modulatory
control of submaximal and maximal lengthening contractions.
We evoked motor responses by electrical stimulation at the
cervicomedullary junction (CMEP) and by TMS over the
primary motor cortex during submaximal and maximal isometric and lengthening contractions in biceps brachii (BB) and
brachioradialis (BR) muscles. Based on the assumption that the
corticospinal tract is free from presynaptic control (Jackson
et al. 2006; Nielsen and Petersen 1994) and that the CMEP for
the elbow flexor muscles contains a dominant monosynaptic
component (Petersen et al. 2002), changes in CMEPs reflect
alterations at the spinal motoneuron pool itself, whereas
changes in the ratio of CMEP to MEP area reflect effects at the
motor cortex.
The fact that CMEPs are considered to be free of presynaptic
inhibition (in contrast to H-reflexes) and work well during
maximal contractions [in contrast to motor potentials evoked
by transcranial electric stimulation (TES)], makes the comparison of MEPs with CMEPs the most direct possibility to
Address for reprint requests and other correspondence: M. Gruber, Dept. of
Training and Movement Science, University of Potsdam, Am Neuen Palais 10,
14469 Potsdam, Germany (E-mail: [email protected]).
The costs of publication of this article were defrayed in part by the payment
of page charges. The article must therefore be hereby marked “advertisement”
in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
INTRODUCTION
2030
0022-3077/09 $8.00 Copyright © 2009 The American Physiological Society
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Gruber M, Linnamo V, Strojnik V, Rantalainen T, Avela J.
Excitability at the motoneuron pool and motor cortex is specifically
modulated in lengthening compared to isometric contractions. J Neurophysiol 101: 2030 –2040, 2009. First published January 28, 2008;
doi:10.1152/jn.91104.2008. Neural control of muscle contraction
seems to be unique during muscle lengthening. The present study
aimed to determine the specific sites of modulatory control for
lengthening compared with isometric contractions. We used stimulation of the motor cortex and corticospinal tract to observe changes at
the spinal and cortical levels. Motor-evoked potentials (MEPs) and
cervicomedullary MEPs (CMEPs) were evoked in biceps brachii and
brachioradialis during maximal and submaximal lengthening and isometric contractions at the same elbow angle. Sizes of CMEPs and
MEPs were lower in lengthening contractions for both muscles (by
⬃28 and ⬃16%, respectively; P ⬍ 0.01), but MEP-to-CMEP ratios
increased (by ⬃21%; P ⬍ 0.05). These results indicate reduced
excitability at the spinal level but enhanced motor cortical excitability
for lengthening compared with isometric muscle contractions.
NEURAL CONTROL OF LENGTHENING MUSCLE CONTRACTIONS
identify modulatory actions at the cortical versus spinal level
during strong muscle contractions (for review, see Taylor and
Gandevia 2004). In the present study, we hypothesized that
specific modulations at the motoneuron pool and motor cortex
would be evident for lengthening compared with isometric
contractions.
METHODS
Nine people (aged 22– 47, 3 females) participated in the study.
They had no history of serious injuries of the right hand, arm, or
shoulder and no seizures, neurosurgery, or metal or electronic implants in their skull. The participants were familiar with the testing
device and had previously experienced lengthening contractions with
the intention to resist maximally. However, they were not engaged in
athletic or specific eccentric training at the time of the measurements.
Ethical approval
All subjects gave their informed consent prior to the measurements.
The experiments were approved by the ethics committee of the
University of Jyväskylä and conformed to the standards set by the
latest revision of the Declaration of Helsinki.
The measurement of elbow flexor torque was similar to that
described in earlier papers (Komi et al. 2000; Linnamo et al. 2006).
Participants sat in a chair. The lever arm was equipped with a strain
gauge transducer. This transducer was adjusted for each participant to
avoid any pain during maximal contractions. The distance between the
axis of rotation of the lever arm and the force transducer was
measured to calculate torque. Measurements were performed isometrically at a 110° elbow angle and dynamically at an elbow angle
between 80 and 140° with a constant velocity of 1 rad/s (see Fig. 2).
Passive torque curves were recorded prior to the measurements to
measure the gravity-dependent torques produced only by the weight
of the arm. The EMG signals were checked throughout the whole
movement to ensure that no muscle activity was present. After the
experiments, these passive torque curves were subtracted from measured torque curves during the experiment to obtain active torque
values.
Electromyography
Electromyographic (EMG) activity was recorded from the BB, BR
and triceps brachii (TB) muscles of the right arm using self-adhesive
electrodes (Blue Sensor N-00-S, Medicotest). The electrodes were
adjusted on the muscle belly in accordance with the underlying
muscle fiber direction (interelectrode distance ⫽ 20 mm; interelectrode resistance ⬍2 k⍀). Alignment of the electrodes was checked
according to the shape of the M-wave. It was ensured that each subject
showed a smooth bipolar shaped M-wave during 50% and maximal
voluntary contractions. The signals were filtered (10 Hz to 1 kHz),
amplified (500 times, amplifier NL824-153, Digitimer, Welwyn, Garden City, UK) and sampled at 5 kHz through an AD-Interface (CED
2701 with Signal software, Cambridge Electronic Devices, Cambridge, UK).
Stimulation methods (Stim)
Motor responses were recorded for elbow flexor muscles (BB and
BR) with stimulation at the brachial plexus to evoke maximal compound muscle action potentials (maximal M-wave ⫽ Mmax), stimulation between the mastoids (cervicomedullary stimulation ⫽ CMS) to
activate the cervicomedullary junction and evoke short-latency reJ Neurophysiol • VOL
sponses in the arm muscles (CMEP), and TMS over the motor cortex
to elicit MEPs.
BRACHIAL PLEXUS STIMULATION. Single electrical stimuli were
delivered to the brachial plexus to evoke maximal M-waves (Mmax) in
BB and BR (pulse duration ⫽ 1 ms; constant current; MEB-5304K,
Nihon Kohden, Tokyo, Japan). The cathode (Unomedical, 4560M;
Unomedical, Stonehouse, UK) was placed in the supraclavicular fossa
and the anode (V-Trodes, No. 2702, 2 in round, Mettler Electronics,
Anaheim, CA) on the acromion. The intensity used to evoke Mmax at
rest in both muscles was doubled (40 –70 mA) for stimulation during
the experiments.
Transmastoid electrical stimulation was delivered via electrodes (Unomedical, 4560M; Unomedical) attached to the skin over the mastoid processes with the cathode
on the left side (pulse duration ⫽ 100 ␮s; constant current; DS7A,
Digitimer, Welwyn). Such stimulations are able to activate axons in
the corticospinal tract at the level of the cervicomedullary junction. As
a result of this activation, short-latency responses in the arm muscles,
termed CMEPs, can be observed (for review, see Taylor and Gandevia
2004). To be sure that activation did not shift toward the ventral roots
of motor axons when stimulation intensity and contraction strength
were increased, we analyzed latencies of CMEPs carefully throughout
the experiment. Stimulator output (180 –395 mA) was set during 50%
isometric MVC to produce responses with peak-to-peak amplitudes in
BB of 66 ⫾ 9% of Mmax (BR: 57 ⫾ 20% Mmax).
CERVICOMEDULLARY STIMULATION.
TRANSCRANIAL MAGNETIC STIMULATION. MEPs were evoked in
the BB and BR muscles of the right arm (Magstim 200, SA34 0HR;
Magstim, Whitland, UK). A circular coil (Magstim S/N135, 14 cm
OD) was positioned over the motor cortex of the left hemisphere to
evoke MEPs. It was orientated to induce a posterior-to-anterior
current in the underlying cortical area. The coil was adjusted during
rest to determine the optimal position. Thereafter it remained in this
position throughout the whole experiment. This was ensured by
attaching the coil to a helmet and securing the helmet to the chair
(3-point fixation). In addition, the scalp was marked and positions of
markings in relation to the coil were checked during and after each
contraction. Stimulus intensities ranged between 40 and 60% of
maximum stimulator output. Intensities were adjusted at 50% of
isometric MVC to produce MEPs in BB with peak-to-peak amplitudes
of 69 ⫾ 7% Mmax (BR: 50 ⫾ 8% Mmax).
The intensity of TMS was individually adjusted during 50% isometric MVCs to ensure that motor responses following CMS and
TMS were comparable in size [amplitudes and areas of MEPs and
CMEPs were not statistically different; BB amplitudes: P ⫽ 0.166;
BB areas: P ⫽ 0.097; BR amplitudes: P ⫽ 0.248; BR areas: P ⫽
0.602; paired Student t-test]. After adjusting the intensity, two stimuli
with a 20% higher intensity were evoked to ensure that preset CMEP
and MEP peak-to-peak amplitudes could increase by ⬎10% of their
value (normalized to Mmax). This ensured that MEPs and CMEPs were
below their plateau values during 50% isometric MVCs (input-output
property in the corticospinal tract) to identify both decreased and increased responsiveness at the motor cortex during lengthening and
maximal contractions. The stimulation intensities for both TMS and CMS
were then kept constant throughout the experiment.
Experimental procedures
After subjects gave informed consent to participate in the study,
EMG electrodes were placed on the muscles and interelectrode resistance was checked. Thereafter electrodes for brachial plexus stimuli
were place. Then participants were positioned in an adjustable chair.
The trunk was fixed to the chair with safety seat belts. The forearm
was supinated and fixed to a custom-made isokinetic elbow extension
device (Komi et al. 2000). The elbow joint was aligned to the axis of
rotation to prevent any movement of the lower arm in relation to the
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Muscle torque
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M. GRUBER, V. LINNAMO, V. STROJNIK, T. RANTALAINEN, AND J. AVELA
throughout the whole experiment and prevent participants from bearing the weight of the helmet and coil (Fig. 1A).
During the experiment, participants performed lengthening and
isometric elbow flexions in a dynamometer at 50 and 100% of MVC.
Lengthening contractions commenced after initial isometric contraction to the preset activation level. For contractions at 50% of MVC,
the participants were asked to align the actual torque displayed on an
oscilloscope in front of them with a line that was set to exactly 50%
of MVC. Five hundred milliseconds to 1 s after they reached the target
level (50% MVC), the ergometer was triggered, and participants
performed the lengthening contraction with the intention of maintaining a constant level of effort. For maximal contractions, participants
were instructed to contract maximally and to maintain this level until
the end of the lengthening phase. The ergometer was again triggered
500 ms to 1 s after the participants reached their isometric MVC. The
initial isometric contraction was performed at an elbow angle of 80°.
In the case of a following elbow extension, participants were instructed to maintain a constant contraction intensity throughout the
lengthening phase. All isometric measurements and stimulations were
performed at an elbow angle of 110° (see Fig. 2). After contractions
of 50% MVC a break of ⱖ1 min was allowed. After maximal
contractions a break of ⱖ2 min was mandatory.
To minimize the total number of contractions, participants performed three trials for each target torque level. This resulted in a total
of 48 contractions [3 repetitions * 2 contraction intensities (maximal
and submaximal) * 2 contraction modes (isometric and lengthening) *
4 (3 stimuli) stimulation at the brachial plexus, stimulation between
FIG. 1. Experimental apparatus, stimulation sites, study protocol, and parameters of
evoked (electromyographic) potentials.
A: experimental apparatus for isometric and
lengthening elbow flexions with stimulation
sites for transcranial magnetic stimulation,
cervicomedullary stimulation and brachial
plexus stimulation. B: participants performed 3 blocks of 16 contractions. In each
block, contractions with contraction mode
[isometric (ISO) and lengthening (LEN)],
contraction intensity [maximal voluntary
contraction (MVC) and 50% of MVC] and
stimulation [electrical stimulation of brachial plexus, electrical stimulation of the
corticospinal tract (CMS), transcranial magnetic stimulation of the motor cortex (TMS)
or no stimulation (control)] were performed
in a randomized order. C: the area of evoked
potentials was calculated between cursor 1,
which was set at the initial deflection from
baseline after stimulation (Stim), and cursor
2, which was set at the second horizontal
crossing (see Martin et al. 2006). The latency of the evoked potential was defined as
the time between stimulation and cursor 1,
and the duration of the evoked potential as
the time between stimulation and cursor 2.
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level arm of the system. The upper body was positioned so that
participants performed elbow flexion and extension as naturally as
possible. The maximal range of movement was set to an elbow angle
between 80 and 140° (180° ⫽ fully extended elbow) and secured with
mechanical stoppers. After positioning, participants were allowed to
do some submaximal contractions to become accustomed to the
testing procedure. Thereafter three isometric MVCs were performed
at elbow angles of 110 and 80°. The mean maximal torque values of
these trials were calculated, and the 50% isometric MVC torques were
displayed as two lines on an oscilloscope along with the actual torque
during the subsequent experiment.
M-waves were then evoked at rest at an elbow angle of 110° in BB
and BR by stimulating the brachial plexus. We analyzed peak-to-peak
amplitudes and determined the stimulation intensity that evoked Mmax
in resting conditions, whereby no further increase in M-wave occurred
with increasing stimulation intensity. This intensity was then doubled,
and three stimulations were performed at this intensity during isometric contractions of 50% MVC. Peak-to-peak amplitudes of Mmax were
analyzed, and the mean value was calculated. Thereafter electrodes
were placed for CMS and the stimulation intensity was adjusted to
result in CMEP peak-to-peak amplitudes of ⬃70% of Mmax during
isometric contractions of 50% MVC. Finally, we positioned the
helmet and the coil for TMS and adjusted the stimulation intensity to
evoke MEPs of similar amplitudes to CMEPs. The coil was attached
to the helmet to ensure that the position of the coil remained constant
relative to the skull during the measurements. The helmet was upheld
by a device mounted to the chair to maintain a constant head position
NEURAL CONTROL OF LENGTHENING MUSCLE CONTRACTIONS
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FIG. 2. Group data showing background electromyographic activity (BGA) of biceps brachii (BB) and brachioradialis (BR) muscles, torque and elbow angle.
Normalized and averaged data of all trials from all participants are shown from 1 s prior to stimulus for both isometric and lengthening contractions. Data for
isometric contractions are in gray and for lengthening contractions in black. Left: submaximal contractions; right: maximal contractions. 1, the time of
stimulation. Lengthening and isometric contractions were matched for torque during the 1st 400 ms (1s to ⫺600 ms). Differences in absolute BGA and torque
values during this interval are mainly because of normalization to Mmax and MVC for a 110° angle. Please note the immediate increase in BGA in both muscles
at the beginning of muscle lengthening (2). This increase is more pronounced in the submaximal condition, and almost reaches the electromyographic (EMG)
level of maximal contractions (onset of EMG rises for BB and BR are displayed in the figure). The sudden increase in torque at the start of the lengthening
movement resulted from inertia of the isokinetic machine (see Linnamo et al. 2003).
the mastoids, stimulation over the motor cortex (⫹ control)]. These
contractions were performed in three blocks, each with 16 unique
contractions. In each of these blocks, contractions were randomized.
Participants were informed about the contraction mode and thereafter
instructed to aim for 50% MVC or MVC torque level, which was
displayed on a monitor at eye level. Participants were not informed
about the upcoming stimulation.
In three of the nine subjects, nine additional isometric contractions
were performed at the end of the protocol to evoke Mmax, CMEPs, and
MEPs at matched background activity (BGA) levels during submaximal contractions. To find the appropriate isometric contraction
strength, the BGA of BB and BR for submaximal lengthening contractions was analyzed. Thereafter the subjects had to contract isometrically while the torque level displayed on the screen was steadily
increased until BGA level of the isometric contractions matched the
J Neurophysiol • VOL
50% lengthening contractions. After we adjusted torque levels individually, stimulations were applied in a randomized order during
isometric contractions with ⱖ2-min rest between contractions.
Data analysis
Peak-to-peak amplitudes and areas of Mmax, CMEPs, and MEPs
were calculated between the initial deflection (⫽ latency of evoked
potential) of the EMG from baseline to the second crossing of the
horizontal axis (⫽ duration of evoked potential; Fig. 1C). Results for
peak-to-peak amplitudes and areas were similar but only areas are
reported. For each participant, the mean areas of three trials at a given
contraction intensity and mode were calculated. CMEPs and MEPs
were normalized to the mean Mmax values recorded during contractions of the same intensity and mode. Torque was normalized to the
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2034
M. GRUBER, V. LINNAMO, V. STROJNIK, T. RANTALAINEN, AND J. AVELA
mean of the three isometric MVC contractions without stimulation.
Torque levels and background EMG activities (BGA as mean amplitude voltage) for BB, BR, and TB were calculated over a 100 ms
period prior to stimulation. BGA was normalized to the mean Mmax
values (calculated as mean amplitude voltage) of the evoked potential
recorded during contractions of the same intensity and mode.
Repeatability and stability
Statistics
Group data are presented as means ⫾ SD unless otherwise stated.
Paired t-test were used to reveal differences in torque and BGA of BB,
BR, and TB in time intervals of 100 ms prior to stimulations for
lengthening versus isometric contractions, and to compare latencies
and durations of evoked potentials, as well as sizes of CMEPs and
MEPs (normalized to Mmax) for submaximal isometric contractions.
One-way repeated-measures (ANOVA) with Bonferroni corrected
post hoc tests were used to test differences between contraction modes
(isometric and lengthening), intensities (submaximal and maximal),
and muscles (BB and BR) for normalized CMEPs, MEPs, and MEPto-CMEP ratios. The level of significance was set to P ⱕ 0.05
(2-tailed).
RESULTS
Torque and BGA
For lengthening contractions, a marked increase in EMG
level lasting ⬃200 ms was observed after the onset of muscle
lengthening (Fig. 2). For submaximal lengthening contractions
with 50% preactivation level, EMG started to rise at 20.0 ms
for BB and 22.6 ms for BR after the onset of movement. EMG
increased almost to the level exhibited in maximal contractions. For maximal lengthening contractions, it was not possible to determine a distinct onset of the EMG rise. Elbow angles
were identical at the time of stimulation. Torque, BB, BR, and
TB BGA for isometric MVCs did not differ from lengthening
MVCs, whereas contractions performed with 50% preactivation, and the effort required to maintain this 50% level throughout the lengthening contraction, resulted in significantly increased torques and BGA levels in BB and BR, but reduced
activity of the TB (Table 1).
Evoked potentials
Stimulations were delivered at the brachial plexus and between
the mastoids as well as over the motor cortex to elicit potentials in
J Neurophysiol • VOL
P
Torque, Nm
MVC ISO
MVC ECC
50% ISO
50% ECC
BGA BB, mV
MVC ISO
MVC ECC
50% ISO
50% ECC
BGA BB, % Mmax
MVC ISO
MVC ECC
50% ISO
50% ECC
BGA BR, mV
MVC ISO
MVC ECC
50% ISO
50% ECC
BGA BR, % Mmax
MVC ISO
MVC ECC
50% ISO
50% ECC
BGA TB, mV
MVC ISO
MVC ECC
50% ISO
50% ECC
50.2 ⫾ 18.2
52.4 ⫾ 20.0
27.0 ⫾ 10.3
32.9 ⫾ 13.2
.297
0.55 ⫾ 0.26
0.56 ⫾ 0.21
0.27 ⫾ 0.20
0.41 ⫾ 0.15
.473
7.8 ⫾ 3.0
7.6 ⫾ 2.9
3.5 ⫾ 1.7
5.1 ⫾ 2.1
.785
0.36 ⫾ 0.09
0.34 ⫾ 0.08
0.19 ⫾ 0.08
0.28 ⫾ 0.08
.303
8.3 ⫾ 2.3
7.7 ⫾ 3.0
3.6 ⫾ 1.1
5.8 ⫾ 1.5
.425
0.11 ⫾ 0.08
0.10 ⫾ 0.07
0.05 ⫾ 0.02
0.03 ⫾ 0.01
.056
.002
.004
.007
.011
.007
.005
Differences between maximal voluntary muscle torque obtained at a 110
elbow angle (angle of stimulation) for isometric (MVC ISO) and lengthening
(MVC ECC) contractions and submaximal isometric (50% ISO) and lengthening (50% ECC) contractions were tested with paired Student t-tests.
the EMG of BB and BR during maximal and submaximal isometric and lengthening contractions. Figure 3 shows superimposed M-waves, CMEPs, and MEPs in one subject for BB. For
this participant, MEPs and CMEPs were reduced for lengthening
contractions compared with isometric contractions, whereas Mmax
remained unchanged. Figures 4 and 5 display CMEP and MEP
sizes in relation to corresponding torque and prestimulus EMG
levels respectively for the same subject. CMEPs and MEPs for
BB and BR for this subject were lower for lengthening contractions (E and 䊐) compared with isometric contractions (F and 䊐).
For the group (n ⫽ 9), latencies and durations of Mmax,
CMEPs, and MEPs in BB and BR did not differ between
lengthening and shortening contractions (P always ⬎ 0.05;
Table 2). Moreover, no differences were found between normalized sizes of CMEPs and MEPs for BB (P ⫽ 0.097) and
BR (P ⫽ 0.602) during isometric contractions at 50% MVC.
Results of group comparisons for CMEPs, MEPs, and MEPto-CMEP ratios are shown in Fig. 6.
Sizes of CMEPs
Analysis of repeated measures for CMEPs revealed no
differences between maximal and submaximal contractions
(P ⫽ 0.240) or between BB and BR (P ⫽ 0.334), but CMEPs
were significantly lower for lengthening contractions compared
with isometric contractions (43 ⫾ 11 and 59 ⫾ 14% Mmax; P ⫽
0.001). Bonferroni-corrected post hoc tests showed that sizes
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One decisive point of the present study was to compare unfatigued
isometric and lengthening maximal contractions. Our pilot studies
showed that not more than ⬃20 –30 maximal contractions could be
performed without inducing fatigue, even with 2 min breaks between
the contractions. As an additional limitation, no more than three
stimulations for each contraction mode, intensity, and stimulation type
could be elicited. Therefore we had to ensure high repeatability and
stability of the performed trials. Analyses were performed separately
for stimulations as well as contraction modes and intensities. Values
for Cronbachs Alpha showed high repeatability throughout the experiment for BGA BB (0.855– 0.961), BGA BR (0.702– 0.923), torque
(0.942– 0.999), Mmax BB (0.970 – 0.985), Mmax BR (0.909 – 0.968),
CMEP BB (0.889 – 0.952), CMEP BR (0.838 – 0.938), MEP BB
(0.731– 0.945), and MEP BR (0.826 – 0.950). Univariate tests of
repeated measures for these parameters using time (3) as the withinsubjects factor and comparing the first, second, and third trials
resulted in no statistically significant differences (P always ⬎ 0.05).
TABLE 1. Torque and background activity (BGA) of biceps
brachii (BB), brachioradialis (BR), and triceps brachii (TB)
NEURAL CONTROL OF LENGTHENING MUSCLE CONTRACTIONS
2035
of CMEPs were lower in both submaximal (BB by 26 ⫾ 27%;
P ⫽ 0.015 and BR by 19 ⫾ 23%, P ⫽ 0.029) and maximal
lengthening contractions (BB by 27 ⫾ 27%; P ⫽ 0.006 and BR
by 27 ⫾ 43%; P ⫽ 0.015) compared with isometric contractions.
Sizes of MEPs
Analysis of repeated measures for MEPs revealed no differences between maximal and submaximal contractions (P ⫽
0.577), but MEPs were significantly lower for BR compared
with BB (58 ⫾ 12 vs. 69 ⫾ 14% Mmax; P ⫽ 0.008) and during
lengthening contractions compared with isometric contractions
(58 ⫾ 16 vs. 68 ⫾ 9% Mmax; P ⫽ 0.007). Bonferroni-corrected
post hoc tests showed that sizes of MEPs were lower during
maximal lengthening contractions for BB by 19 ⫾ 23% (P ⫽
0.041) and for BR by 20 ⫾ 14% (P ⫽ 0.002) compared with
maximal isometric contractions. For submaximal contractions
the respective post hoc tests did not show any significant
differences (P values always ⬎ 0.05).
J Neurophysiol • VOL
MEP-to-CMEP ratios
For MEP-to-CMEP ratios, analysis of repeated measures
revealed no differences between contraction intensities (P ⫽
0.342) or between BB and BR (P ⫽ 0.340), but MEP-to-CMEP
ratios were significantly higher for lengthening compared with
isometric contractions (1.27 ⫾ 0.41 vs. 1.05 ⫾ 0.21; P ⫽
0.039). However, Bonferroni-corrected post hoc tests showed
no significant differences for specific comparisons (P values
always ⬎ 0.05).
Evoked potentials for submaximal contractions
with matched BGA
Additional measurements at slightly higher isometric contraction strength were performed in three of the nine participants to match BGA to that of submaximal lengthening contractions (BB: 0.34 ⫾ 0.18 mV for isometric and 0.35 ⫾ 0.18
mV for lengthening; BR: 0.23 ⫾ 0.07 mV for isometric and
0.25 ⫾ 0.06 mV for lengthening; TB: 0.05 ⫾ 0.01 mV for
isometric and 0.06 ⫾ 0.02 mV for lengthening). Torque values
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FIG. 3. Superimposed EMG responses of a single subject to brachial plexus (Mmax), cervicomedullary electrical (CMEP) and transcranial magnetic stimulation
(MEP) for biceps brachii. Left: isometric contractions (ISOs); right: lengthening contractions (LENs) of the same target torque. - - -, timing of stimulation. [uarro],
onset of Mmax (top traces), CMEPs (middle traces), and MEPs (bottom traces). 2, 2nd reflex response that can follow corticospinal tract stimulation during
maximum or near maximum voluntary contractions (see Taylor et al. 2001). For this subject, the response was regularly observed during isometric MVCs but
only for 1 of the 3 lengthening maximal contractions. Please note that CMEPs and MEPs are lower during lengthening compared with isometric contractions
whereas maximal M-waves do not differ.
2036
M. GRUBER, V. LINNAMO, V. STROJNIK, T. RANTALAINEN, AND J. AVELA
FIG. 4. Relationship between size of evoked potential (MEP and CMEP)
and level of prestimulus torque of 1 subject. Data obtained from biceps brachii
and brachioradialis for isometric and lengthening contractions are superimposed. A: CMEPs; B: MEPs. Please note that responses evoked during
isometric contractions in biceps brachii (F) and brachioradialis (■) are bigger
than those obtained during lengthening contractions (E for biceps brachii and
䊐 for brachioradialis), whereas torque level is higher in lengthening than
isometric contractions. Same subject as in Fig. 3.
were higher for lengthening (63.3 ⫾ 1.0% MVC) than isometric (54.2 ⫾ 0.6% MVC) contractions. Mean values for CMEP
and MEP sizes expressed in % Mmax were higher in isometric
(CMEP BB: 66 ⫾ 9 and BR 66 ⫾ 8; MEP BB: 73 ⫾ 11 and
BR 51 ⫾ 4) than lengthening contractions (CMEP BB: 53 ⫾
10 and BR 46 ⫾ 09; MEP BB: 51 ⫾ 13 and BR 42 ⫾ 6).
DISCUSSION
This study provides new data on the neural control of
lengthening muscle contractions. We compared areas of
CMEPs and MEPs between lengthening and isometric contractions to differentiate between mechanisms acting at the spinal
and cortical levels. The size of the MEP reflects excitability
and neuron properties at the motor cortex and the spinal
motoneuron pool, whereas the CMEP only relates to spinal
motoneuron properties. It should be acknowledged that MEPs
and CMEPs may activate motoneurons differently because the
MEP involves multiple volleys and the CMEP only a single
volley. Therefore motor-unit potentials after TMS are more
dispersed and some motoneurons may discharge more than
J Neurophysiol • VOL
FIG. 5. Relationship between size of evoked potential (MEP and CMEP)
and level of prestimulus EMG of 1 subject. Same subject and figure layout as
in Fig. 4. Bigger responses during isometric contractions compared with
lengthening contractions were found over the whole range of prestimulus EMG
levels.
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once, which can affect the size of potentials averaged from
surface EMG (Keenan et al. 2006). However, recent studies
provide no evidence that these differences might affect the
susceptibility of CMEPs or MEPs to changes in spinal excitability specifically. Martin et al. (2006) found comparable
changes in MEPs and CMEPs with changes in contraction
strength and stimulation intensity, which indicate similar responses of MEPs and CMEPs to changes at the spinal level.
Taylor et al. (2002) reported an occlusive interaction between
responses to CMS and descending action potentials evoked by
TMS at short interstimulus intervals in BB. This observation is
consistent with the two stimuli activating some of the same
corticospinal axons for this muscle. Based on the assumption
that CMEPs and MEPs of similar size recruit the motoneuron
pool of BB and BR in a similar manner, lower CMEPs and
increased MEP-to-CMEP ratios in lengthening compared with
isometric contractions indicate that properties of motoneurons
as well as of neurons located at the motor cortex were modulated differently during lengthening versus isometric contractions in the present study. These modulations will be discussed
with respect to contraction strength and possible underlying
mechanisms.
NEURAL CONTROL OF LENGTHENING MUSCLE CONTRACTIONS
TABLE 2. Latencies and durations [ms] of the evoked potentials
in BB and BR during isometric and lengthening contractions
at MVC and 50%
Mmax
Latency BB
Latency BR
Duration BB
Duration BR
CMEP
Latency BB
Latency BR
Duration BB
Duration BR
MEP
Latency BB
Latency BR
Duration BB
Duration BR
MVC ISO
MVC ECC
50% ISO
50% ECC
4.4 ⫾ 0.4
6.2 ⫾ 0.8
23.3 ⫾ 2.4
22.2 ⫾ 5.2
4.4 ⫾ 0.5
6.2 ⫾ 0.5
23.6 ⫾ 2.3
22.8 ⫾ 4.1
4.6 ⫾ 0.4
6.4 ⫾ 0.5
25.4 ⫾ 2.3
23.7 ⫾ 5.2
4.4 ⫾ 0.3
6.4 ⫾ 0.7
23.9 ⫾ 2.7
23.5 ⫾ 1.7
8.2 ⫾ 0.4
10.1 ⫾ 0.5
20.5 ⫾ 4.8
20.0 ⫾ 5.6
8.3 ⫾ 0.6
10.1 ⫾ 0.8
18.0 ⫾ 3.3
17.0 ⫾ 2.4
8.2 ⫾ 0.6
10.3 ⫾ 0.8
22.5 ⫾ 1.9
21.1 ⫾ 4.1
8.3 ⫾ 0.4
10.1 ⫾ 0.5
20.3 ⫾ 3.2
20.4 ⫾ 1.5
10.9 ⫾ 0.4
12.5 ⫾ 1.0
24.1 ⫾ 3.9
22.7 ⫾ 5.3
10.5 ⫾ 0.5
12.5 ⫾ 0.7
23.8 ⫾ 4.3
22.7 ⫾ 4.9
11.0 ⫾ 0.6
12.7 ⫾ 0.7
27.8 ⫾ 2.6
25.7 ⫾ 4.8
10.8 ⫾ 0.8
12.4 ⫾ 1.0
24.4 ⫾ 2.7
24.0 ⫾ 2.8
Latencies and durations were compared between isometric and lengthening
contractions of the same intensity level by paired Student’s t-tests 2 tailed). No
significant differences were found (P always ⬎.05). MEP, motor-evoked
potential; CMEP, cervicomedullary MEP.
During maximal lengthening contractions, higher torques
compared with isometric contractions could be expected because short-range stiffness should contribute considerably to
overall muscle forces for the lengthening muscles (Rack and
Westbury 1974). Unlike in vitro muscle preparations but in
accordance with previous in vivo studies (Aagaard et al. 2000;
Komi et al. 2000; Linnamo et al. 2002, 2003, 2006; Seger and
Thorstensson 2000; Westing et al. 1991), lengthening torques
did not exceed isometric torques for the whole range of motion
in the present study (Fig. 2 and Table 1). Studies that used
superimposed mechanical (Webber and Kriellaars 1997), peripheral electrical (Babault et al. 2001; Beltman et al. 2004;
Pinniger et al. 2000; Seger and Thorstensson 2000; Westing
et al. 1990), or TMS (Loscher and Nordlund 2002) showed that
the torque of maximal lengthening contractions can be significantly increased. Therefore the disparity between the expected
and effectively measured torque was mainly attributed to an
activation failure that, in consequence, limits recruitment
and/or discharge rates of motor units during maximal lengthening contractions. The fact that CMEPs but not MEP-toCMEP ratios were lower during maximal lengthening compared with isometric contractions indicates that any activation
failure in the present study was located exclusively at the spinal
level (Fig. 6). Consequently, we suggest that voluntary descending drive from the motor cortex toward the muscle did
not limit force production during maximal voluntary lengthening contractions.
Submaximal contractions
Lengthening submaximal contractions were started with a
preactivation level of 50% MVC at an 80° angle and performed with the intention of maintaining the level of effort
throughout the lengthening phase of the contraction (Linnamo et al. 2002). The lengthening phase was characterized
by steep rises in BB and BR EMG with onsets that are well
in line with latencies of stretch reflexes in these muscles (see
J Neurophysiol • VOL
Table 2 in Yamamoto and Ohtsuki 1989). Therefore it can
be assumed that EMG increases were caused by discharges
of muscle spindles as a consequence of muscle lengthening
(Burke et al. 1978). This increase was much more pronounced in submaximal compared with maximal precontractions, which is in accordance with the fact that Ia input
could recruit additional motoneurons in submaximal conditions but not during maximal contractions where the whole
motoneuron pool should already be recruited (Kukulka and
Clamann 1981). Higher EMG and torque levels were observed throughout the lengthening movement (Fig. 2). Bonferroni-corrected post hoc tests showed no significant increases for MEP-to-CMEP ratios, and therefore the present
study provides no direct evidence for a higher cortical
excitability during submaximal lengthening contractions,
whereas reduced CMEPs indicate that modulatory changes
occurred exclusively at the motoneuron pool (Fig. 6). It
should be noted that unlike in maximal contractions, BGA
of BB, BR, and TB, as well as torque, were not matched for
submaximal lengthening and isometric contractions (Fig. 2
and Table 1). We evoked CMEPs with an area of approx.
60% Mmax during 50% MVC and found no differences in
size during MVCs with the same stimulation intensity (Fig.
6). This is well in line with the results of Martin et al. (2006;
their Fig. 3A). Based on their results, CMEP and MEP sizes
could be expected to increase from 50% MVC up to ⬃75%
MVC for such a stimulus intensity but then decrease to
reach approximately the sizes measured at 50% MVC for
MVC itself. As a consequence, the present study’s submaximal lengthening contractions, which resulted in slightly
higher torques and BGA for BB and BR compared with
isometric contractions of 50% MVC, should not result in
reduced but rather in increased CMEPs and MEPs. To
enable a more direct measure of this behavior, we added an
additional protocol. In three subjects, we matched BGA
during submaximal isometric (⬃54% MVC) and lengthening (⬃63% MVC) contractions and found similarly lower
values for CMEPs and MEPs. Our data suggest that reductions in CMEPs and MEPs during lengthening contractions
were not primarily a result of varying BGA (Fig. 5).
This conclusion is in line with previous studies that
compared rather weak lengthening and shortening contractions for elbow flexor muscles (Abbruzzese et al. 1994;
Sekiguchi et al. 2001). Abbruzzese et al. (1994) investigated
evoked potentials after TMS and TES as well as peripheral
nerve stimulation (H-reflex via the radial nerve) in the BB
and BR muscles. During weak lengthening contractions,
motor responses for TES, TMS, and H-reflex were significantly reduced compared with shortening contractions at
similar levels of BGA. Such a uniform variation across
contraction types between evoked potentials that involve
cortical as well as peripheral pathways indicates that the
mechanisms are probably located at the motoneuron pool
itself. While Abbruzzesse et al. (1994) used a constant
stimulus intensity (1.5 times motor threshold at rest) for
TMS, Sekiguchi et al. (2001) investigated the input-output
property of the corticospinal tract (Devanne et al. 1997).
MEP sizes for all stimulus intensities were significantly
smaller during weak lengthening contractions for BR,
whereas there were no differences regarding threshold levels. These results indicate mechanisms that are able to
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Maximal contractions
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M. GRUBER, V. LINNAMO, V. STROJNIK, T. RANTALAINEN, AND J. AVELA
suppress the subliminal fringe of the corticospinal tract
during lengthening contractions. The comparison of CMEPs
and MEPs in the present study provides more direct evidence that these mechanisms may act mainly at the spinal
level.
Modulatory mechanisms during maximal
lengthening contractions
Recently the influence of discharge rate and recruitment of
motor units during voluntary isometric contractions on the size
of CMEPs and MEPs was discussed in great detail (Martin
J Neurophysiol • VOL
et al. 2006). Martin et al. (2006) found a concurrent increase
followed by a reduction in CMEP and MEP size when increasing contraction strength of isometric elbow flexion from 50%
MVC up to MVC. Furthermore, they observed that the size of
either CMEPs or MEPs depended not only on contraction
strength but also on stimulus intensity. Both findings are well
in line with predictions drawn from motoneuron modeling
(Matthews 1999). For the comparison of maximal contractions
in this study, it seems appropriate to assume that all motoneurons of BB and BR were recruited when we evoked the motor
responses (Kukulka and Clamann 1981). Based on this assumption, alterations in CMEP and MEP areas could be related
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FIG. 6. Group data showing areas of
MEPs and CMEPs normalized to Mmax obtained for maximal and submaximal isometric
contractions compared with those obtained
during lengthening contractions. Data from 9
subjects are pooled and mean ⫾ SE values are
shown. A: submaximal contractions; B: results
for maximal contractions. Left: evoked potentials for BB during isometric and lengthening
contractions; right: results for BR. Analysis of
repeated measures revealed decreased CMEPs
and MEPs (P ⬍ 0.01) and increased MEP-toCMEP ratios (P ⬍ 0.05) during lengthening
compared with isometric contractions. In post
hoc analysis, CMEPs were always lower in
lengthening compared with isometric contractions, whereas MEPs only decreased during
maximal contractions. Post hoc analysis revealed no differences for comparisons between
MEPs during submaximal contractions and
MEP-to-CMEP ratios. Evoked potentials in
BB and BR displayed the same behavior.
#P ⬍ 0.05 CMEPs or MEPs different to isometric.
NEURAL CONTROL OF LENGTHENING MUSCLE CONTRACTIONS
J Neurophysiol • VOL
The present study did not aim to clarify specific alterations in
recruitment and firing properties. However, reduced CMEPs
showed that the responsiveness of motoneurons was reduced for
any peripheral or corticospinal input in lengthening compared
with isometric contractions. This behavior cannot be explained by
higher firing rates of motoneurons during lengthening compared
with isometric contractions, which suggests that inhibition of
motoneurons may mainly operate at the spinal level. There are
various mechanisms that could diminish spinal excitability. However, the comparison of CMEPs and MEPs provides no evidence
that could favor any of these mechanisms nor does it exclude any
as a possible candidate. According to previous studies, the potential mechanisms most likely to explain inhibition of spinal motoneurons may be Ib afferent inhibitory input from Golgi tendon
organs (Aagaard et al. 2000) and the setting of motoneuron
excitability by supraspinal structures (Abbruzzese et al. 1994;
Sekiguchi et al. 2001).
From a functional perspective, the purpose of inhibiting motoneurons during lengthening muscle contractions could be to control
muscle force. For submaximal contractions, this mechanism may
enable the adjustment of muscle force to the requirements of the task,
thus facilitating proper execution of the movement. For maximal
lengthening contractions, this mechanism is powerful enough to
reduce maximal eccentric force values considerably. However, any
inhibition of motoneurons should decrease the number of active
motor units and thus increase the stress (force per unit area) on these
units above the level perceived during maximal isometric contractions (Please note that eccentric MVC was similar to isometric MVC
in the present study). The weakest half-sarcomeres in active myofibrils would take up most of the total length change until the point of
no myofilament overlap. As a result, in these half-sarcomeres, the
force in passive structures would balance the force produced by still
intact cross-bridges of adjacent sarcomeres (for review, see Proske
and Morgan 2001). For repeated lengthening contractions, this could
lead to a considerable number of disrupted sarcomeres, causing
muscle damage that has been demonstrated to occur after this kind of
exercise (Avela et al. 1999; Chen et al. 2003; Crameri et al. 2007;
Nosaka et al. 2002). It can be speculated that increased maximal
eccentric strength accompanied by increased agonistic EMG, as has
been reported to occur after only one training session (Linnamo
2002), is related to neural adaptations that result in the removal of
some of the inhibitory setting at the spinal level (Aagaard et al. 2000).
Moreover, such adaptations can explain increased voluntary maximal
eccentric strength and increased agonistic EMG after high-intensity
strength training (Aagaard et al. 2000) and in eccentrically trained
athletes (Amiridis et al. 1996).
In conclusion, the present study showed that the responsiveness
of motoneurons was reduced for any peripheral or corticospinal
input in lengthening compared with isometric contractions, indicating inhibition of spinal motoneurons. The observed reduction
in CMEPs indicates that spinal excitability was considerably
lower in lengthening than isometric contractions, whereas a moderate increase in MEP/CMEP ratio indicates that cortical excitability was slightly higher. We suggest that increased cortical
excitability results in extra excitatory descending drive during
muscle lengthening to compensate for spinal inhibition. This
indicates changes in neural control of muscle activity for both
spinal and cortical sites in lengthening compared with isometric
contractions.
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to changes in discharge rates of already recruited motoneurons.
Once recruited, a motoneuron should become effectively more
refractory and therefore less excitable by increasing the discharge rate as a result of its afterhyperpolarization trajectory.
This was predicted by mathematical models (Jones and Bawa
1997; Matthews 1999) and tested in single human motoneurons
by peripheral stimulation of the Ia afferents (Jones and Bawa
1995) as well as TMS of the corticospinal tract (Olivier et al.
1995). Recently Martin et al. (2006) mainly attributed their
observation of decreasing CMEPs with increasing isometric
contraction strength from 75% MVC toward MVC to this
mechanism. They argued that once all motoneurons are recruited with a given stimulus intensity, a further increase in
contraction strength can only decrease the overall response.
Thus for maximal contractions, the reduction in CMEPs found
in the present study during lengthening contractions could
reflect increased discharge rates of already recruited motoneurons. However, this is rather unlikely because higher firing
frequencies for lengthening contractions compared with isometric contractions should result in much higher maximal
torques as suggested by classical in situ stimulation data
reported by Rack and Westbury (1974). Moreover, in studies
that examined single motor units at given torque levels during
lengthening contractions compared with isometric contractions, unchanged (Pasquet et al. 2006) or even lower discharge
rates were reported (Howell et al. 1995; Tax et al. 1989).
Reduced firing frequencies could explain the deficit in maximal
torque but assuming full motoneuron recruitment these alterations should result in increased and not in reduced CMEPs
(Martin et al. 2006).
A possible explanation for reduced CMEPs is selective recruitment of motoneurons. If we assume selective recruitment of
motoneurons as a neural strategy to control overall motor output
during lengthening contractions, the inhibitory control has to be
very powerful to ensure that these motoneurons will not become
recruited by maximal voluntary drive or enhanced Ia afferent
input during muscle lengthening. In that case, inhibition of specific motoneurons could be so strong that it was not possible to
recruit them via corticospinal volleys used in the present study.
Consequently, this would explain decreases in CMEP and MEP
sizes, respectively. However, there is no direct evidence for
selective recruitment during maximal lengthening contractions.
Until now, such behavior was only observed during submaximal
or rather weak lengthening contractions when a light weight has to
be lowered (Howell et al. 1995; Nardone et al. 1989). Nardone
et al. (1989) described selective recruitment of high-threshold
motor units in soleus and gastrocnemius muscles during rather
weak lengthening contractions. Howell et al. (1995) found similar
recruitment patterns for the human first dorsal interosseus muscle.
It was speculated that the functional advantage could be a silencing of low-threshold motor units and concurrently reduced reflexive muscle contractions via Ia afferent contributions, which allows
central mechanisms more freedom to control muscle contraction
(Nardone et al. 1989). It should be noted that such a control
scheme might not only depend on contraction strength but could
be muscle specific as well. In recent studies, no specific derecruitment of low-threshold motoneurons was observed for BB or
tibialis anterior during lengthening compared with isometric or
shortening contractions (Kossev and Christova 1998; Pasquet
et al. 2006; Sogaard et al. 1996; Stotz and Bawa 2001; Tax et al.
1989).
2039
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M. GRUBER, V. LINNAMO, V. STROJNIK, T. RANTALAINEN, AND J. AVELA
ACKNOWLEDGMENTS
The authors gratefully acknowledge M. Ruuskanen and S. Roivas for
technical support and N. Cronin for proofreading this manuscript.
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