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DOI 10.1007/s00221-001-0960-1
R E S E A R C H A RT I C L E
Received: 8 February 2001 / Accepted: 24 October 2001 / Published online: 16 January 2002
Springer-Verlag 2002
Abstract Stretch reflexes were evoked in the submaximally activated ankle extensors during sinusoidal length
perturbations. A mean stretch reflex (SR) amplitude
SRindex and FDSRArel can be proposed as a tool to analyze changes in reflex excitability, which can accompany
a process of neuromuscular plasticity. In order to validate the procedure, the proposed parameters were quantified in a case study before and after a period of plyometric training.
Keywords Reflex excitability Sinusoidal length
perturbation Stretch reflex Voluntary activation
Triceps surae
D. Lambertz F. Goubel C. Prot ()
Universit de Technologie de Compigne,
Dpartement de Gnie Biologique, CNRS UMR - 6600,
60205 Compigne cedex, France
e-mail: chantal.perot@utc.fr
Tel.: +33-3-44234392, Fax: +33-3-44204813
Introduction
Typically, stretch reflexes are obtained by imposing
joint perturbations either in force or in length while a
subject maintained a voluntary tonic activation. Reflex
responses of the triceps surae to imposed sinusoidal
force perturbations on the ankle joint were first described by Agarwal and Gottlieb (1977). Considering the
mechanical properties of the ankle joint a priori as a linear input-output system, imposed force perturbations induce changes in the resulting displacement. Thus, using
force perturbations, both variations in frequency and
in length can influence the stretch reflex amplitude
(Agarwal and Gottlieb 1980). Stretch reflexes in response to imposed perturbations in length have also been
studied using different methods: random perturbations
(Kearney and Hunter 1983), large and sudden ramp displacements (Kearney and Chan 1982; Toft et al. 1991;
Kirsch and Kearney 1993), or sinusoidal perturbations at
different frequencies (Rack et al. 1978; Neilson and
McCaughey 1981; Evans et al. 1983). So, during imposed sinusoidal length perturbation at a given level of
preactivation and at different frequencies, changes in reflex activities only depend on the variations in frequency, providing that muscle stretching is carefully controlled.
The aim of the cited stretch reflex studies was often
focused on the eventual mechanical importance of the
stretch reflex. In expressing joint stiffness as a force resisting an angular displacement, a large joint stiffness
provides good position control, notably during postural
tasks, which are generally non-stable, and favors the application of additional forces. With regard to the neurophysiological properties, the generation of the additional
forces depends on the reflex response. When mechanically induced, this reflex depends, firstly, on the elastic
properties of the musculo-tendinous structures in series
with the muscle spindles (Rack et al. 1983) and, secondly, on the supraspinal control (Sinkjaer 1997; Mirbagheri
et al. 2000). In turn, reflex excitability contributes to regulate muscle stiffness. Furthermore, both reflex excit-
90
ability and mechanical properties are affected by neuromuscular plasticity. Some evidence has been given that
training and disuse induce: (1) neural adaptation, including reflex excitability (Sale 1988; Duchateau 1995;
Enoka 1997), and (2) mechanical adaptation, including
the elastic properties (Cornu et al. 1997; Lambertz et al.
2001) of the neuromuscular system.
In the present study we propose a new characterization of the stretch reflex obtained during sinusoidal
length perturbations at different levels of muscle preactivation and at different frequencies. Such a new characterization offers the possibility to compare the reflex excitability of different muscles and to follow changes in
the reflex excitability of a given muscle during a period
of training or disuse, independently of the maximal activation capacities of the muscle, which are also altered by
such changes in the functional demand. The new parameters proposed in the present study were firstly quantified for a slow muscle (soleus), known to be highly excitable, and for less excitable muscles (gastrocnemii).
Secondly, a case study illustrated the physiological interest of the proposed parameters, quantified for the soleus
muscle before and after so-called plyometric training.
The intent of this type of training is to increase the instantaneous explosive power output as required during
short-term efforts such as sprinting or jumping. Then, the
proposed parameters were used to assess changes in reflex excitability due to such a physical conditioning.
cle and, for the Sol, 2 cm below the insertion of the gastrocnemius
muscles on the Achilles tendon. EMGs were recorded differentially, amplified, and bandpass filtered (11,000 Hz).
Furthermore, an additional experiment was done on a college
student who volunteered for this part of the present study. The aim
of this case study was to validate the proposed parameters as a
tool to analyze changes in reflex excitability before and after
8 weeks of plyometric training.
Experimental protocol
The torque from a maximal voluntary contraction (MVC) was determined in plantarflexion under isometric conditions while the
subject was asked to develop maximal contraction against the
actuator. The true MVC level of the day, corresponding to the best
torque, was determined by choosing the greatest of three attempts
to generate the maximal voluntary effort. Each of these attempts
lasted 4 s and were 2 min apart in time. Then, two experimental
paradigms were applied.
Firstly, stretch reflex activities at different contraction levels
were studied at a single frequency. Therefore, sinusoidal length
perturbations were imposed on the ankle joint at a constant frequency of 16 Hz while the subject maintained a submaximal plantarflexion torque, varying from 10% to 70% of MVC in steps of
10%. The displacement amplitude was fixed at 3 peak-to-peak.
This non-physiological high frequency was chosen because at this
frequency the musculo-articular system works under inertial conditions, which means that the dynamic stiffness of the musculoarticular system is constant whatever the level of contraction and
so, does not interact with the stretch reflex response (Matthews
1994).
Secondly, stretch reflex activities were characterized over a
range of frequency and a single level of contraction. Therefore,
sinusoidal length perturbations of 3 peak-to-peak were applied at
different frequencies ranging from 6 to 16 Hz in steps of 1 Hz.
During this part of the experiment the subject maintained the plantarflexion torque at 50% of MVC.
To perform these tasks the subject was instructed to hold a
constant level of force production by matching an oscilloscope
trace despite the oscillations in the torque signal. To facilitate this
task, the torque traces used as visual feedback consisted in a lowpass filtering of the output torque. Thus, all subjects were able to
keep their level of force production at the target value without any
difficulty, whatever the imposed frequency. The use of a frequency
range from 6 to 16 Hz should also eliminate the possibility for the
subject to resist the stretch voluntarily or to do tracking movements, since the high frequency tracking range was seldom above
7 Hz (Bennett 1994; Cathers et al. 1996). Data sampling started
when the subject reached the target value and sinusoidal perturbations were applied 1 s later. The sinusoidal oscillations lasted 4 s.
The subject relaxed as soon as the perturbation stopped and resting periods of at least 1 min were observed between the different
perturbation sequences to prevent muscle fatigue.
As for the additional experiment, sinusoidal perturbations were
imposed according to the two experimental paradigms before and
after the period of training. In each experimental situation, the
subject maintained contraction levels evaluated by considering the
actual MVC of the day. Furthermore, supramaximal electrical
stimulations were achieved in order to get the maximal motor
direct response (Mmax) of the Sol. The mean amplitude of the Sol
), expressed by the ratio between duration and area,
Mmax (M
max
was used to normalize stretch reflex activities and, thus, to take into account the different conditions of skin and surface electrodes
impedance in signals recorded on different days.
Data processing and analysis
Background activity (BGR) was defined as mean amplitude of the
rectified EMG recorded during the first second of sampling, i.e.,
before the sinusoidal perturbations were imposed. Then, as pro-
91
Fig. 1 A Raw data set of electromyogram (EMG) responses
to sinusoidal oscillations (arrow
indicates the beginning of the
lengthening phase). B, C Effect
of data processing on the stretch
reflex evoked during sinusoidal
perturbations, for the soleus
(Sol, thin lines) and the gastrocnemii (Gas, thick lines). In
B, background activities (BGR)
are degraded and the stretch reflex consisted essentially in the
more time-locked short latency
component. In C, rectification
is done prior to averaging.
Consequently, BGR activity remains present and the stretch
reflex appears as the short and
medium latency components.
Data obtained at 9 Hz and for
50% of maximal voluntary contraction (MVC)
posed by Evarts and Vaughn (1978), averaging prior to rectification was chosen to favor the quantification of time-locked or periodic EMG signals mixed with non-correlated EMG background
activity, such as the early component of a stretch reflex. The efficiency of this data processing is illustrated in Fig. 1, showing that
averaging of unrectified data favored the quantification of the
short latency response, whereas the later, less synchronized component was degraded by such a procedure.
Therefore, stretch reflex responses collected during sinusoidal
perturbations were analyzed as follows. Data were first inspected
visually to keep a number of successive periods where the required voluntary torque remained almost constant despite the imposed perturbations. After this windowing, the EMGs of Sol, GL,
and GM muscles were averaged over the remaining periods and
then rectified. GM and GL were summed up to express the gastrocnemii (Gas) activity. Since the EMGs of Sol, GM, and GL
were first averaged and then rectified, no correction of BGR was
necessary at this stage (see Fig. 1). However, this method can only
be used after the experimenter has carefully controlled that BGR
does not change notably during the muscle stretch.
Stretch reflex (SR) areas were determined by integrating the
averaged EMG over the time interval corresponding to the expected burst of reflex activity, i.e., as reported for the plantarflexors
inside a time interval which started and ended around 35 and
60 ms, respectively. In the present study, onset and offset of the
EMG burst were pointed out by the experimenter to compute latency and duration of the stretch reflex, respectively. In doing so,
the prominent peak of the reflex burst corresponded to the SR amplitude. Latency was always referenced
at the onset of the length
ening phase. A mean SR amplitude (SRA value was also calculat-
ed as the ratio between SR area and SR duration in order to consider possible influences of reflex duration. This was justified
since the literature indicates differences in reflex duration according to stretch modalities (Gottlieb et al. 1995; Morita et al. 1998).
Firstly,
the accuracy of the SR parameters (amplitude, area,
and SRA) was attested studying
the relationships between SR amplitude and, SR area and SRA, respectively. Then, the comparison
between both correlation coefficients
r should reflect possible effects of SR duration on SR area and SRA.
Secondly, stretch reflex activities were studied with regard
to
the background
level,
BGR.
For
this
purpose
Sol
and
Gas
SRA
to establish normalized SRABGR and SRArel BGR relationships. BGRmax was achieved from the best MVC measurement of
the day.
Thirdly, SRA and SRArel frequency relationships were established. In the case of a linear regression between these parameters, the slope of the relationships can be calculated. However, this
method required that the correlation coefficient r matched a critical value. Thus, in order to avoid a dependency on the correlation
coefficient r, another parameter was proposed to characterize the
distribution of the stretch reflex over the different applied
frequencies.
This
parameter
represents
the
area
under
the
SRA
or
92
data set of the first experimental paradigm before and after the
training period. Secondly,
according
to the first experimental
paradigm, normalized SRA and SRArel values were calculated
and
related to BGR/BGRmax. Thirdly, normalized FDSRA and
FDSRArel were quantified according to the second experimental
paradigm.
Statistics
A Students one-sample t-test was used to verify that mean values
were significant for the population. Based on these findings, a multiple regression analysis was used to investigate
the relations
among SR amplitude, SR duration, SR area, and SRA. Therefore, a
partial correlation procedure was applied which consisted in computing partial correlation coefficients rp which describe the linear
relationship between two variables while controlling for the effects
of one or more additional variables. Differences in Sol and Gas reflex activities for the two experimental paradigms were tested by
using Students t-test for independent samples. Data are presented
as mean SEM. Statistical significance was accepted at P<0.05.
Results
Pattern of the stretch reflex
Influence of BGR
In response to a sinusoidal length perturbation of low
amplitude and high frequency (16 Hz) the Sol and the
Gas muscles exhibited a rhythmic burst of activity at
each lengthening phase of the sinusoidal perturbation.
The stretch reflex consisted of a single burst of activity.
Its mean latency was 35.40.5 and 33.10.6 ms for Sol
and Gas, respectively. Mean SR duration for Sol did not
change significantly with the target torque (16.81.6 and
15.91.4 ms from the lowest to the highest contraction
level, respectively). In contrast, mean SR duration for
Gas changed with the level of BGR from 18.62.6 ms at
the lowest contraction to 14.41.3 ms at the highest contraction. For each level of contraction (10% to 70%
SR amplitude and SRA, were highly correlated as attested by the linear relationships established between these
parameters (Fig. 2A, B). A possible influence of SR duration was statistically analyzed using the partial correlation coefficients method. For this purpose, SR amplitude
was used as control variable. Then, the correlation matrix was calculated for each muscle. As for the Sol, no
significant correlations were found between SR duration
SR area
SRA
a Denotes
Sol
SRA
rp=0.792
P<0.05a
SR duration
Gas
SRA
SR duration
rp=0.604
P>0.05
rp=0.103
P>0.05
rp=0.610
P>0.05
rp=0.797
P<0.05a
rp=0.044
P>0.05
Influence of frequency
Stretch reflex activities, evoked when maintaining 50% of
MVC, were always observed at frequencies higher than
9 Hz. For some subjects, no reflex activities were detect-
93
Table 2 Partial correlation
coefficients matrix between SR area,
SR duration, and SRA for the soleus (Sol) and the gastrocnemii
(Gas) at different frequencies (616 Hz) and at a constant level of
MVC (50%). This matrix reveals that SR duration of Gas influences reflex activities when SR area is used
SR area
SRA
Sol
SRA
rp=0.229
P>0.05
SR duration
Gas
SRA
SR duration
rp=0.557
P>0.05
rp=0.481
P>0.05
rp=0.286
P>0.05
rp=0.670
P<0.05
rp=0.418
P>0.05
was used as the control variable. Then, the correlation matrix revealed no significant correlation between SR area
and SRA neither for Sol nor for Gas. On the other hand,
SR duration and SR area were correlated for Gas but not
for Sol (see Table 2), indicating that Sol reflex activities
seemed to be independent of duration when the perturba
tion frequency changed. Thus, SRA will allow the comparison between reflexes which are different in duration.
In the subsequent sections, the stretch reflex will be ana
lyzed considering only SRA values.
amplitude, SR area, and SRA were calculated. Mean values were found to be significant for the population
(P<0.05) as attested by Students one-sample t-test. Then,
the influence of SR duration was estimated by the analysis
94
Fig. 4 Relationships between SRA (A) and SRArel (B), and the
normalized background (BGR/BGRmax), respectively, for the soleus (Sol; circles) and the gastrocnemii (Gas; squares). BGR (10%
to 70% of MVC) was quantified during the first second preceding
the perturbations (16 Hz). In B, the slopes of the linear relationships defined SRindex. For Sol, SRindexis 1.39 and for Gas, SRindex
is 0.85. Data are represented as mean SEM, which are representative for the population at P<0.05
that some subjects exhibited SRAfrequency relationships with a correlation coefficient which did not
match the critical value for a linear regression analy
sis (P>0.05). In such a case, the link between SRA
and frequency was approached by considering the area
1
1.350.32 mV s and mean FDSRA for Gas was
Fig. 5 Relationships between SRA (A) and SRArel (B), and frequency, respectively, for the soleus (Sol; at the back) and the gastrocnemii (Gas; in front). BGR (50% of MVC) is quantified during
FDSRArel has to be considered when studying the frequency dependency of the stretch reflex at different levels of BGR.
95
Additional experiment
SRArel. As one can see, SRA after training varied markedly over the range of activation (see Fig. 7A), whereas
excitability due to training were assessed using the negative slope which, in turn, is also independent of changes
in BGR/BGRmax. The negative slope was found to be
steeper after training than before training (12.17 after
training vs 4.04 before training).
Thirdly, according to the second experimental para
96
Discussion
In the present study a detailed electromyographic analysis of the stretch reflex led to introduce new parameters,
which can be useful for studying changes in muscle reflex excitability when changes in functional demands
(for example, a period of training or disuse), and thus in
motor drive, occur. Stretch reflex activities can be
evoked in different ways, such as sinusoidal perturbations. Knowing that muscle spindles are also sensitive to
slow and slight perturbations, sinusoids were often chosen because they involve no sudden impulsive movements that might stimulate, in a synchronized manner, a
large number of sensory receptors in an artificial and
non-physiological way (Rack et al. 1978; Evans et al.
1983).
The reflex activities described in the current experiments were evoked by a controlled sinusoidal length perturbation of low amplitude and at different frequencies.
These activities can be considered as a stretch reflex,
mediated via a spinal reflex pathway, since their latencies were within the range of the response to an Achilles
tendon tap, i.e., somewhat shorter than those reported in
other studies when using large ramp displacement at low
The data processing chosen (averaging prior to rectification) favored the analysis of the short latency component
of the stretch reflex (Evarts and Vaughn 1978; see also
Fig. 1). If a reflex study should also include the quantification of longer latency components of the stretch reflex,
EMGs should be rectified prior to averaging, and thus,
further BGR activity correction should be taken into account.
The SR duration of Gas was influenced by both the
level of muscle activation and the frequency, whereas
Sol SR duration was never modified by one of these parameters. The lower Gas SR duration at high levels of
muscle activation or at high frequency, accompanied by
97
to analyze stretch reflex activities, SRA values should facilitate the comparison of reflex excitability, which can
be different in duration or recorded in different muscles.
98
no changes in the slope occurs (i.e., in the case of parallel slopes). If these changes in functional demand are accompanied, as is often the case, with changes in submaximal muscle activation, it will be recommended to express data in relative values. In the present study the
FDSRArelBGR/BGRmax relationship can also be proposed as a new index (FDSRindex) to describe changes
in reflex excitability due to changes in functional demand when further individual levels of BGR are used.
FDSRindex should emphasize the evaluation of reflex
excitability even when changes in maximal motor drive
occur and can be proposed to follow, for example, the
time-course of rehabilitation.
In conclusion, the present study showed a simple description of the human stretch reflex evoked by sinusoidal
length perturbations, which represented a good tool to
test muscle reflex excitability. Sinusoidal length perturbations applied at different levels of BGR and at different
frequencies led us to propose new parameters to characterize reflex excitability, notably the frequency distribu
tion of the stretch reflex (FDSRArel). These parameters
could be useful to follow the time-course of the reflex excitability of muscles as for example, during rehabilitation
or training. Additionally, sinusoidal perturbations can
also be used to study mechanical properties of muscle. In
this way, sinusoidal perturbations can be used to study
both mechanical and neurophysiological parameters. It
appears then that a combined study of these parameters
99
would provide a better understanding of the consequences of, for example, a specific training program or a microgravity environment (Lambertz et al. 2001) in terms of
postural and movement control (Mirbagheri et al. 2000).
Finally, two indexes were proposed in order to characterize reflex excitability independently of changes in maximal activation. The first one, SRindex, gives the reflex excitability at a high frequency where the mechanical response of the ankle joint system does not interact with the
reflex response. On the other hand, the second index, FDSRindex, takes into account the frequency response, and
thus, the intrinsic mechanical properties of the neuromuscular system including muscle spindles. These indexes
should then facilitate the comparison of reflex excitability
between different muscles and different subjects. Moreover, the proposed parameters can be used when other
types of controlled perturbations are used (for example,
ramp displacements at different angular velocities). However, in the view of an SRindex evaluation, the perturbation
velocity should be high enough to ensure that the ankle
joint system works under inertial conditions.
Acknowledgements This study was supported by grants from the
Centre National dEtudes Spatiales (CNES) and the Ple GBM
Prinatalit-Enfance de la Rgion Picardie.
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