R. H. Westgaard, P. Bonato and K. A.

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J Neurophysiol 88:1177-1184, 2002.

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Low-Frequency Oscillations (⬍0.3 Hz) in the Electromyographic
(EMG) Activity of the Human Trapezius Muscle During Sleep
R. H. WESTGAARD,1,2 P. BONATO,2 AND K. A. HOLTE1
1
Norwegian University of Science and Technology, N-7491 Trondheim, Norway;
and 2NeuroMuscular Research Center, Boston University, Boston Massachusetts 02215
Received 14 November 2000; accepted in final form 8 May 2002
Westgaard, R. H., P. Bonato, and K. A. Holte. Low-frequency
oscillations (⬍0.3 Hz) in the electromyographic (EMG) activity of the
human trapezius muscle during sleep. J Neurophysiol 88: 1177–1184,
2002; 10.1152/jn.00823.2000. The surface electromyographic (EMG)
signal from right and left trapezius muscles and the heart rate were
recorded over 24 h in 27 healthy female subjects. The root-mean-
square (RMS) value of the surface EMG signals and the heartbeat
interval time series were calculated with a time resolution of 0.2 s.
The EMG activity during sleep showed long periods with stable mean
amplitude, modulated by rhythmic components in the frequency range
0.05– 0.2 Hz. The ratio between the amplitude of the oscillatory
components and the mean amplitude of the EMG signal was approx-
imately constant over the range within which the phenomenon was
observed, corresponding to a peak-to-peak oscillatory amplitude of
⬃10% of the mean amplitude. The duration of the periods with stable
mean amplitude ranged from a few minutes to ⬃1 h, usually inter-
rupted by a sudden change in the activity level or by cessation of the
muscle activity. Right and left trapezius muscles presented the same
pattern of FM. In supplementary experiments, rhythmic muscle ac-
tivity pattern was also demonstrated in the upper extremity muscles of
deltoid, biceps, and forearm flexor muscles. There was no apparent
association between the rhythmic components in the muscle activity
pattern and the heart rate variability. To our knowledge, this is the first
time that the above-described pattern of EMG activity during sleep is
documented. On reanalysis of earlier recorded trapezius motor unit
firing pattern in experiments on awake subjects in a situation with
mental stress, low-FM of firing with similar frequency content was
detected. Possible sources of rhythmic excitation of trapezius mo-
toneurons include slow-wave cortical oscillations represented in de-
scending cortico-spinal pathways, and/or activation by monoaminer-
gic pathways originating in the brain stem reticular formation. The
analysis of muscle activity patterns may provide an important new
tool to study neural mechanisms in human sleep.
INTRODUCTION
It has been known for some time that low-level muscle
activity occurs during sleep in association with slow wave
components in the electroencephalographic (EEG) signal and
that this muscle activity is inhibited during rapid-eye-move-
ment (REM) sleep (cf. Pompeiano 1967; Steriade and McCar-
ley 1990 for reviews). It is also recognized that patients with
pain of a putative musculoskeletal origin, where muscle activ-
ity may be part of the pain induction process, often suffer from
poor sleep (e.g., fibromyalgia, chronic fatigue syndrome, myo-
Address for reprint requests: R. H. Westgaard, Institute of Industrial Eco-
nomics and Technology Management, Norwegian University of Science and
Technology, N-7491 Trondheim, Norway.
www.jn.org 0022-3077/02 $5.00 Copyright © 2002 The American Physiological Society
J Neurophysiol
88: 1177–1184, 2002; 10.1152/jn.00823.2000.
fascial pain syndrome) (Goldenberg 1993; McCain and Scudds
1988). We therefore conducted a study with surface electro-
myographic (EMG) recordings from the trapezius muscles to
investigate possible association between EMG activity during
sleep and sleep quality, including subjectively experienced
overnight discomfort or pain. In a few supplementary record-
Downloaded from jn.physiology.org on January 6, 2009
ings, upper extremity muscles were included. The study is an
extension of earlier work in this field and included also daytime
monitoring of EMG and heart rate (Jensen et al. 1993a; Vas-
seljen and Westgaard 1995; Westgaard et al. 2001).
Inspection of the EMG recordings confirmed that periods
with sustained low-level muscle activity were present during
sleep. The root-mean-square (RMS) value of the detected
EMG activity showed a characteristic pattern, featuring periods
where the EMG signal amplitude was remarkably stable over
periods lasting as long as 1 h. There was little short-term
variation in the EMG data, with the striking exception of the
consistent appearance of low-frequency amplitude oscillations
at frequencies ranging from ⬃0.05 to 0.2 Hz. Although rhyth-
mic muscle activity has been illustrated in many studies per-
taining to sleep physiology (e.g., Arduini et al. 1963; Glenn
and Dement 1981; Marchiafava and Pompeiano 1964), to our
knowledge this activity has not been properly analyzed before.
The purpose of this paper is to present this phenomenon,
describe its characteristics, and discuss possible neurophysio-
logical mechanisms in the generation of this muscle activity
pattern.
METHODS
Subjects and data recording
Twenty-seven female subjects (mean age 45.1 yr, range 31– 62 yr)
participated in the study following written informed consent. The
subjects were recruited from a health-care center with elderly people
(health-care personnel without heavy physical work tasks) and from a
shopping center (retail personnel). The purpose of the study, as
explained to the subjects, was to further the insight in work-related
shoulder pain by comparison of muscle activity during work and after
working hours. About half of the subjects had experienced moderate
shoulder pain during the last 6 mo but were still working, the other
half reported no shoulder pain. No one had diagnosed sleep disorders.
During daytime (⬃9 AM to 5 PM), the working hours were spent in
retail customer service or providing health care for patients that in
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.
1177
1178 R. H. WESTGAARD, P. BONATO, AND K. A. HOLTE
most cases were physically able to provide for themselves. Outside
working hours the subjects carried out their normal activities without
receiving any instructions as to preferred or restricted activities. They
were not instructed with respect to the use of caffeine or other
stimulants. Another five females, recruited from the same subject
base, participated in supplementary experiments with simultaneous
recordings of trapezius and upper extremity muscles.
Electrocardiographic (EKG) and surface EMG signals were con-
tinuously recorded over a 24-h period. A lightweight, battery-powered
data monitor equipment (Physiometer, Premed) with data storage
provided by a flash card mounted in a pocket computer (HP 200LX,
Hewlett-Packard) was used as the recording device. Electrodes for
recording the EKG signal were placed in standard positions across the
chest. The surface representation of the cardiac potential with Q, R,
and S peaks (the QRS complex; Malik and Camm 1995) was detected.
The intervals between the R peaks (RR intervals) were derived on a
beat-by-beat basis. The surface EMG activity from left and right
trapezius muscles was monitored by bipolar electrode pairs and in-
cluded a ground electrode (10- to 800-Hz bandwidth). The EMG
electrodes (circular with diameter 6 mm, Blue Sensor, E-10-vs, Medi-
cotest A/S) were placed on a line from the C7 vertebra to the acromion
process. The medial electrode was placed 2.5 cm lateral to the mid-
point of the line and the inter-electrode distance was 20 mm. This
electrode placement was shown to produce a stable EMG signal even
with electrode movement in relation to the underlying muscle (Jensen
et al. 1993b). The ground electrode was placed on the spine of the C7
vertebra. The EMG recording device was used to process the raw
signals by calculating the RMS value using a 0.1-s time window. EKG
and EMG data were stored on the HP computer at a sampling rate of
J Neurophysiol • VOL
10 Hz. On transfer of data to a stationary PC, the time resolution was
reduced to 0.2 s by averaging adjacent data points.
Before the ambulatory recording, a maximal voluntary contraction
(MVC) in 90° arm abduction was performed twice by the subject to
acquire the maximal EMG amplitude. This was used as a reference
value to calibrate the EMG response during the ambulatory recordings
(% EMGmax) (Jensen et al. 1996). Daytime results are not reported in
this paper; however, the trapezius muscle activity was generally low
in the awake state with the median EMG activity level for most
subjects in the range 2–5% EMGmax (Westgaard et al. 2001). The
duration of the sleep period varied from 4.7 to 8.4 h, mean 6.8 h.
Onset of sleep was determined in these recordings by a sudden change
in the EMG activity pattern from irregular, phasic activity to no
activity, or presenting a dramatically changed pattern with near-
constant EMG amplitude and minimal temporal variation (cf. Fig. 1).
In five subjects, the upper trapezius EMG recordings were supple-
mented by EMG recordings from lower trapezius, deltoid, biceps, and
forearm flexors (flexor carpi ulnaris, flexor digitorum superficialis).
The bipolar electrode pairs were placed on the muscle bellies, and the
EMG signal calibrated by the EMG response in resisted MVCs with
attempted movement in the muscle force direction. In these record-
ings, a strain gauge transducer placed around the chest monitored
respiratory activity.
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The quality of the EMG signal was checked by visual inspection at
the beginning and the end of the recording and by observing the
activity pattern at rest and during a maximal voluntary contraction.
During the recording, an automated quality evaluation procedure
checked for artifacts by detecting slow swings in baseline and/or sharp
transients in the raw signal. Intervals detected by this procedure were
FIG. 1. Electromyographic (EMG) pattern ob-
served during sleep. A: time course of the root-mean-
square (RMS) value of the EMG signal recorded from
the left upper trapezius muscle during sleep. Two
arrows on the bottom of the plot indicate the time
when the subject fell asleep (sleep on) and woke up
(sleep off) respectively. Several intervals of almost
constant EMG amplitude are shown in a range corre-
sponding to values between 1 and 2% EMGmax. Three
arrows and associated shaded areas marked by S1, S2,
and S3 indicate 3 10-min time intervals selected to
illustrate the observed phenomenon more in details
(see bottom). B: the RMS-detected EMG data. C: the
corresponding frequency content. For low-level EMG
activity (bottom left) the square of the magnitude of
the Fourier transform (on the right side) shows a
narrowband component at approximately 1 Hz due to
the EKG interference. For higher EMG activity lev-
els, signal components were generally detected in the
0.05- to 0.2-Hz range.
88 • SEPTEMBER 2002 • www.jn.org
 EMG ACTIVITY OF THE TRAPEZIUS MUSCLE DURING SLEEP 1179

marked and the RMS amplitude examined off-line. Such events were
rare, ⬍0.1% of the data points, unless gross failures due to breakage
of leads or unfastening of electrodes occurred. Of the 27 subjects,
successful sleep recordings were obtained from right and/or left
trapezius in 44 cases, 22 from each side. Both recordings failed in four
subjects, one recording failed in two subjects. In the successful
recordings, the RMS amplitude of data points marked by the artifact
detection procedure rarely deviated significantly from neighboring
data points, and corrective measures were therefore not carried out.
The artifact detection procedure did not respond to interference from
the heartbeat, which could be particularly evident in recordings from
the left upper trapezius during periods with low EMG activity. This
noise component in the EMG signal was dramatically attenuated
through digital filtering in the off-line data processing (cf. next sec-
tion).
Data processing
The time series constituted by the RMS values of the EMG signal
computed over 0.2-s time intervals was first low-pass filtered to
attenuate possible EKG interference. A Chebyshev (type II) low-pass
filter was designed with transition band 0.70 – 0.75 Hz, 40 dB of
attenuation in the stopband, and 1 dB maximum loss in the passband.
an obvious rhythmic component, and the results of the analysis
of these 15 recordings are presented here. There was no ap-
parent association between the EMG response and the shoulder
pain reported by the subjects.
Figures 1 and 2A illustrate the processing of one recording.
The typical appearance of RMS-detected muscle activity dur-
ing sleep is shown in Fig. 1A. Long periods of elevated,
near-invariant EMG activity are interspersed between periods
without discernable activity and short bursts of phasic activity,
presumably due to spontaneous shifts in posture.
Inspection of periods with elevated EMG activity at higher time
resolution reveals low-frequency oscillatory behavior at frequen-
cies ⬍0.2 Hz as outlined by the square of the magnitude of the
Fourier transform of the time series. This is illustrated in Fig. 1B
where three epochs selected from the RMS time series presented
in Fig. 1A are represented (marked S1–S3). These three epochs
have different mean values and frequency contents as pointed out
by the square of the magnitude of their Fourier transform (nor-
malized) shown in the lower panels (Fig. 1, B and C). A trend of
larger amplitude oscillations with increasing mean EMG ampli-
tude is evident. At low activity levels the EMG signal was in some

Downloaded from jn.physiology.org on January 6, 2009

Using a bilinear transformation (with prewarping), the corresponding recordings contaminated by the EKG signal, detected as a distinct
infinite impulse response (IIR) filter was implemented and applied to
the RMS time series as a noncausal filter (i.e., after filtering in the
forward direction, the series was reversed and filtered again).
A series of processing procedures were carried out to characterize
the observed oscillatory phenomenon that appeared to affect the EMG
amplitude. To measure the amplitude of the rhythmic components that
marked the RMS time series, we first selected time intervals in which
the rhythmic components were present and then computed the SD of
the time series over 512-sample epochs with 50% overlap. The esti-
mated values were plotted as a function of the mean RMS value of the
EMG for each epoch.
A second step of the procedure was aimed at characterizing the
RMS time series in the frequency domain. The square of the magni-
tude of the Fourier transform of time intervals of the RMS time series
that showed a rhythmic component was estimated to assess the fre-
quency content of the analyzed signal. In addition, because of the
nonstationarity of the RMS time series, we applied a Choi-Williams
transformation (␴ ⫽ 1) and thus derived the time-frequency distribu-
tion (Williams 1997) of the RMS time series.
To compare the frequency content of the RR time series with that
of the RMS time series, the frequency analysis procedure was also
applied to the RR time series. Both the square of the magnitude of the
Fourier transform of the signal as well as its Choi-Williams time-
frequency representation (␴ ⫽ 1) were computed and compared with
the EMG data. For the recordings including respiratory activity,
time-frequency analysis was applied also to the recorded output of the
strain gauge transducer.
Additional to the processing of the sleep recordings, the firing
pattern of single motor units (MUs) recorded from awake subjects in
an experimental situation with mental stress and minimal body move-
ment was examined. This data set was recorded in an earlier study to
observe motor unit substitution (Westgaard and De Luca 1999). The
modulation of firing pattern in these recordings was investigated by an FIG. 2. Relationship between RMS value of the EMG rhythmic component
autoregressive technique. The frequency content of MU firings was and amplitude of the EMG data. A: the results for the recording illustrated in Fig.
obtained using the Burg method and the order of the model was 1. A linear relationship is shown between the amplitude of the rhythmic compo-
nent that marks the RMS time series and the actual amplitude of the EMG signal.
chosen using the Akaike criterion (Ljung and Glad 1994).
■, data before filtering; E, the results after applying a low-pass filter to attenuate
possible interference from the electrocardiographic (EKG) signal. The regression
lines for these 2 sets of data are also shown. B: the regression lines for all the
RESULTS
recordings with responses higher than 1% EMGmax performed in this study. The
data range is shown by the length of the regression lines with the exception of 1
The RMS amplitude of the EMG recording exceeded 1% case where EMG amplitudes up to 8.5% EMGmax were detected. This plot
EMGmax for ⱖ10 min in 15 (8 from right, 7 from left trapezius) indicates that for most of the recordings, but a few exceptions, the slope of the
of 44 successful recordings. Each of these recordings showed regression line was approximately the same. See text for details.

J Neurophysiol • VOL 88 • SEPTEMBER 2002 • www.jn.org

1180 R. H. WESTGAARD, P. BONATO, AND K. A. HOLTE
peak at ⬃1 Hz in the square of the magnitude of the Fourier
transform of the RMS time series (see Fig. 1, B and C, bottom). A
low-pass digital filter (as described in METHODS) was used to
attenuate this noise component.
Figure 2A shows the scatter plots of RMS oscillatory am-
plitude versus mean RMS amplitude before and after the ap-
plication of the low-pass filtering procedure for the recording
shown in Fig. 1. The data points are selected from segments
with very low EMG activity and from segments with relatively
stable RMS amplitude, up to ⬃2% EMGmax. The effect of
filtering is most evident at low amplitudes, as anticipated. A
further effect of the procedure is to reduce the scatter of the
individual data points from the regression line (R2 ⫽ 0.91
unfiltered, R2 ⫽ 0.98 after filtering). However, the increase in
RMS oscillatory amplitude with increasing RMS mean ampli-
tude is clear in both the filtered and unfiltered data.
All recordings with EMG responses higher than the noise level
showed evidence of the oscillatory behavior illustrated in Fig. 1.
Regression lines of RMS oscillatory amplitude versus mean RMS
amplitude were constructed after filtering, as shown for one sub-
ject in Fig. 2A. The regression lines for all 15 recordings that
reached amplitudes ⬎1% EMGmax are represented in Fig. 2B. The
length of the lines indicates the data range. With the exception of
one recording, the regression lines showed a near-constant asso-
ciation (i.e., slope) between oscillatory amplitude and EMG am-
plitude. The mean slope coefficient is 0.017 ⫾ 0.007 (SD), cor-
responding to approximately a 10% ratio of the peak-to-peak
oscillatory amplitude to mean EMG amplitude. The deviation of
data points from the regression line was low for all subjects; the
mean value of R2 was 0.87 ⫾ 0.11.
The low frequency of the EMG oscillations may suggest an
influence from the sympathetic nervous system as the source of
the motoneuron excitation, by analogy with research on the
heart rate variability (e.g., Malliani et al. 1994; Task Force of
the European Society of Cardiology and the North American
Society of Pacing and Electrophysiology 1996). Rhythmic
activity of sympathetic origin, known from the analysis of
heart rate variability, includes control of circulation (⬇0.1 Hz)
J Neurophysiol • VOL
FIG. 4. Example of heartbeat time series analysis. Bottom: time series
analysis of the intervals between the R peaks (RR time series) in the surface
Downloaded from jn.physiology.org on January 6, 2009
representation of the heartbeat potential (Malik and Camm 1995). Top right:
the square of the magnitude of the Fourier transform of the signal. Top, left:
relative to the time-frequency distribution of the RR time series. The time-
frequency representation indicates that the RR series is a multi-component
signal associated with nonstationarities particularly evident at low frequencies.
The recording was performed simultaneously to the RMS time series presented
in Fig. 3. The comparison of Figs. 3 and 4 indicates that these 2 time series are
constituted by different frequency components. Also, there is no apparent
relationship between the evolution in time of the RMS and RR time series.
and temperature regulation (⬍0.05 Hz). Respiratory activity in
quiet breathing typically has frequencies centered ⬃0.25 Hz.
We therefore compared rhythmic activity in muscle with si-
multaneously recorded heart rate, by examining the square of
the magnitude of the Fourier transform as well as the time-
frequency distribution of the RMS and the RR time series. The
comparison showed that different frequency components con-
tribute to EMG and RR time series.
An example of the analysis is shown in Figs. 3 and 4,
FIG. 3. Example of RMS time-series analysis. Bottom: the
time course of the signal. Right: represents the (normalized)
square of the magnitude of the Fourier transform of the RMS
time series. Top left: the contour plot of the time-frequency
distribution of the RMS time series. The contour plot is obtained
by displaying five contour levels at 10, 30, 50, 70, and 90% of
the maximum of the distribution. The time-frequency represen-
tation shows that the oscillations associated with the EMG AM
are constituted by a single narrowband component, which is
strongly frequency modulated over time.
88 • SEPTEMBER 2002 • www.jn.org
 EMG ACTIVITY OF THE TRAPEZIUS MUSCLE DURING SLEEP 1181

FIG. 5. Simultaneous recording of right and left upper tra-

pezius EMG activity. Bottom: the time course of the RMS time
series recorded from left (A) and right (B) upper trapezius. Top
(A and B): the corresponding time-frequency distributions. It is
indicated that although the average amplitude of the EMG
signal as well as the associated oscillations are of different
magnitude, the time-frequency content of the 2 signals follows
the same pattern.

Downloaded from jn.physiology.org on January 6, 2009

presenting time plots of simultaneous EMG amplitude and RR forearm flexors. Figure 7 shows a 10-min section of recording
time series over a 10-min period, the square of the magnitude with EMG oscillatory modulation in these muscles as well as
of their Fourier transform, and the contour plot of their time- heart rate and respiratory rhythm. A strong oscillatory rhythm
frequency distribution. It is clear that the EMG and the RR ⬃0.2 Hz was observed in biceps and forearm flexors (Fig. 7, D
time series are constituted by different frequency components. and E). Lower trapezius presented the same rhythm in a weaker
Both signals show a nonstationary behavior. The time-fre- response (Fig. 7C) and the rhythm is observed in recordings
quency representation of the EMG time series shows a single from upper trapezius and deltoid (Fig. 7, A and B). However,
component ⬃0.15 Hz that is modulated in frequency in the in these last two muscles, a rhythm at about half the frequency
range between 0.1 and 0.2 Hz. The time-frequency represen- is the more dominant one, presenting a two-component activity
tation of the RR time series shows a quasi-stationary signal pattern in deltoid, whereas a three-component pattern (includ-
component ⬃0.2 Hz and two components ⬍0.1 Hz associated ing respiratory modulation; Fig. 7G) is apparent in upper
with signal nonstationarities. There is no apparent coupling in trapezius. The muscle activity patterns are not coherent with
the dynamic progression of frequency variation between the the modulation of heart rate, with the exception of the respi-
two responses. This observation was confirmed by other re- ratory related rhythmic component, which is dominant in the
cordings.
A similar comparison of EMG responses was made for the
few examples of simultaneous responses (⬎1% EMGmax) in
both trapezius muscles. An example is shown in Fig. 5 where
plots of the RMS time series of right and left trapezius are
shown in the bottom panels while their time-frequency repre-
sentation is presented in the corresponding top panels. The
frequency variations of the EMG AM in the two muscles
appear to follow each other. It should be noted that while the
FM of the EMG amplitude on right and left upper trapezius
follows basically the same pattern, the mean amplitude of the
EMG signal as well as the peak-to-peak amplitude of the
oscillations is clearly different.
The RMS time series was occasionally constituted by two
narrowband components rather than by a single component as
shown in the previous example. One of these observations
when two components were detected in the RMS time series is
reported in Fig. 6. The bottom plot reports the time course of
the signal, whereas the top plot represents its time-frequency
distribution. Two components are shown with similar (but not
always equal) FM.
The two phenomena of multiple frequency components and
FIG. 6. Example of a RMS time series constituted by 2 distinct frequency
same EMG oscillatory behavior of different muscles during components. Bottom: the time course of the signal. Top: time-frequency
sleep are further illustrated in an experiment with simultaneous distribution. The 2 frequency components appear to be associated with similar
recordings from upper and lower trapezius, deltoid, biceps, and but not always equal FM.

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1182 R. H. WESTGAARD, P. BONATO, AND K. A. HOLTE
FIG. 7. Time-frequency analysis of a 10-min section of rhythmic EMG
activity recorded from upper trapezius (A), deltoid (B), lower trapezius (C),
biceps (D), and forearm flexor muscles (E). Heart rate (F) and respiration (G)
were simultaneously recorded. All muscles show a similar, rhythmic modula-
tion centered around a frequency of 0.2 Hz. In addition, upper trapezius and
deltoid show a rhythmic frequency component of ⬃0.1 Hz and the upper
trapezius shows also respiratory modulation. Respiratory modulation is clearly
represented in the RR time series.
RR time series (Fig. 7F) and is also present in the upper
trapezius RMS time series (Fig. 7A).
Finally, evidence of a rhythmic component in the same
frequency range of the above-described observations from
surface EMG recordings was found on investigation of trape-
zius MU activity pattern recorded in a situation with mental
stress (Fig. 8). The MU firing pattern was more irregular
J Neurophysiol • VOL
(noisy) than the surface EMG time series recorded during sleep
thus preventing us from performing time-frequency analysis of
the MU activity; however, by use of an autoregressive tech-
nique, two distinct peaks in the firing rate modulation were
found, centered around 0.25 and 0.1 Hz, respectively. The
higher frequency peak presumably represents respiratory mod-
ulation, while the FM ⬃0.1 Hz may point to activation by the
same premotor pathways that cause muscle activity modulation
during sleep.
DISCUSSION
The phenomenon of low-FM of muscle activity pattern
during sleep was an unanticipated observation made during an
experimental series carried out for different purposes. Impor-
tant features of the phenomenon are a constant ratio of oscil-
latory amplitude to mean EMG amplitude, similar rhythmic
activity in the contralateral trapezius muscles, and the rhythmic
activity corresponds to frequencies typically associated with
sympathetically generated activity but is different from the
sympathetic rhythms manifest in the heart rate variability. We
Downloaded from jn.physiology.org on January 6, 2009
have further demonstrated that muscle activity simultaneously
recorded from upper and lower trapezius muscles and muscles
of the upper extremities may deviate in their time-frequency
patterns and that rhythmic MU activity with a similar fre-
quency content may exist in the awake state, at least in an
experimental situation with mental stress.
Before discussing possible origins of the observed phenom-
enon, we will point out that raw EMG signals were stored and
later examined in some of the later recordings. We can thus
rule out the occurrence of possible artifacts not necessarily
evident from the RMS time series. Also because a continuous
AM is apparent in these raw EMG recordings, the observed
phenomenon may be not attributed to obvious causes (e.g.,
periodic limb movement disorder) that would result in periodic
bursts of EMG activity.
FIG. 8. Frequency content (top) of the firing pattern of trapezius MU
(bottom) in an awake subject during mental stress. Frequency analysis by an
autoregressive technique demonstrates 2 dominant peaks, a presumed respira-
tory component at 0.25 Hz and a component of unknown origin at 0.1 Hz. The
latter component is in the same frequency range as the observations from
surface EMG data recorded during sleep.
88 • SEPTEMBER 2002 • www.jn.org
 EMG ACTIVITY OF THE TRAPEZIUS MUSCLE DURING SLEEP
The time intervals of relatively constant EMG amplitude are
preceded and followed by abrupt changes in the EMG signal.
We suggest that these abrupt changes are related to postural
adjustments. In this case, we expect a displacement between
the surface electrodes and the muscle fibers from which the
EMG data are recorded; however, our previous work suggests
that this displacement is unlikely to affect the EMG amplitude
at the chosen electrode location for trapezius (Jensen et al.
1993b).
Recent developments in sleep research describe physiolog-
ical phenomena that may be associated with the rhythmic
component of modulation of the muscle activity reported in
this study. Because we documented that the FM of the ob-
served rhythmic component is consistent for right and left
trapezius muscles and for muscles further separated, we dis-
cuss in the following “central” mechanisms that could be
related to this phenomenon. We have, however, no explanation
for the phenomenon of dual frequency components appearing
in some, but not all muscles.
The presence of widespread slow waves (⬍1 Hz) in the
cortical electroencephalogram has been reported (Steriade et
al. 1993a– c). These waves are synchronized over wide cortical
regions, including the pyramidal neurons in the motor cortex
(Amzica and Steriade 1995; Contreras and Steriade 1997), and
pyramidal tract neurons present a bursting activity pattern
during sleep (Evarts 1964). The frequency content of the
cortical waves is higher than the muscle activity oscillations
documented in this study, i.e., ⬎0.3 Hz in cats (Steriade et al.
1993b,c) and 0.5–1.0 Hz in humans (Achermann and Borbély
1997). However, the slower envelopes that describe the prev-
alence of slow wave activity and the pattern of occurrence of
spindle activity present a frequency range similar to the rhyth-
mic component of muscle activity documented in this study
(Achermann and Borbély 1997).
The change in frequency content of the modulation of EMG
amplitude during sleep may reflect a changing balance between
slow wave and spindle activity, as the envelopes of these EEG
patterns appear to have different frequencies of dominance. In
the example illustrated in Fig. 5 of Achermann and Borbély
(1997), the first two sleep episodes are dominated by slow
wave activity centered around 0.05 Hz, the last two episodes
are dominated by spindle activity at ⬃0.23 Hz. The envelopes
of rhythmic activity in cortical EEG are associated with similar
fluctuations in the firing of cells in the midbrain and brain stem
reticular formation (Oakson and Steriade 1983; Trulson and
Jacobs 1979).
The muscle activity pattern observed during sleep shows
striking similarities (low-level, invariant activity patterns) to
muscle activity observed in laboratory experiments with in-
duced stress (Wærsted et al. 1996; Westgaard and Bjørklund
1987; Westgaard and De Luca 1999). The surface EMG signal
in these experiments does not usually include an oscillatory
component, however, we here show that the firing rate of
individual motor units may be modulated at frequencies similar
to those observed during sleep. The oscillations in the firing
rate of individual motor units when performing tasks with
induced stress are typically 1–2 pulses per second (pps), cor-
responding to ⬃10% of the mean firing rate. This is in good
agreement with the ratio of EMG amplitude oscillation to mean
EMG amplitude observed during sleep. If all motor units
participated in synchronized firing, a rhythmic component in
J Neurophysiol • VOL
1183
the AM of the surface EMG should be observable. This be-
havior is rarely observed, possibly because many premotor
pathways without oscillatory patterning contribute to the exci-
tation of motoneurons in the awake state.
The observation of low-frequency, rhythmic MU firing
when awake, if confirmed in more extended analyses, may
implicate mechanisms and pathways other than cortical rhyth-
mic activity influencing motoneuron firing through cortico-
spinal pathways. One alternative is activity in premotor mono-
aminergic pathways from the brain stem. These include
serotonergic pathways from the raphe nuclei (Holstege 1991;
Jacobs and Fornal 1997) and noradrenergic pathways from
locus coeruleus (Jacobs et al. 1991). The activity of serotoner-
gic raphe neurons is generally described as regular or “clock-
like” firing at 3– 4 Hz. Slow modulation of this activity at
frequencies similar to those observed in this study is reported
(Montagne-Clavel et al. 1995). The envelope of this FM may
cause AM of the muscle activity pattern with a frequency
content as herein documented. Different activity patterns
within the raphe nuclei (Trulson and Trulson 1982) or between
Downloaded from jn.physiology.org on January 6, 2009
different brain stem structures that show rhythmic activity
patterns (Lydic et al. 1983) may provide clues as to the path-
ways involved in the motoneuron excitation.
It may be considered surprising that the rhythmic muscle
activity, which by frequency content is under influence of the
sympathetic nervous system, is not associated with similar
frequency bands in the heart rate variability. However, the slow
components of the heart rate rhythm are related to specific
control functions, such as respiration and circulation. These
control functions may not be prominently displayed in the CNS
structures that are a putative source of the observed motoneu-
ron excitation during sleep.
Our observation of rhythmic muscle activity may provide an
important window for observation of physiological processes
during sleep, by representing the CNS output to an important
effector organ. The motor output allows a clear description of
dynamic activity components by the time-frequency analysis
utilized in our data processing procedure, and may provide
useful information to supplement, e.g., EEG-recorded activity
patterns.
This study was partially supported by the Norwegian Research Council for
Sciences and Humanities.
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