Exp Brain Res (2014) 232:20112020
DOI 10.1007/s00221-014-3891-3
Research Article
Chronic neck pain alters muscle activation patterns tosudden
movements
ShellieA.Boudreau DeborahFalla
Received: 25 October 2013 / Accepted: 21 February 2014 / Published online: 15 March 2014
Springer-Verlag Berlin Heidelberg 2014
AbstractThe aim of this study was to assess the activa-
tion of the sternocleidomastoid (SCM) and splenius capitis
(SC) muscles in response to unanticipated, full body per-
turbations in individuals with chronic neck pain (NP) and
age-matched healthy controls (HC). Individuals with NP
had a history of NP for 8.97.8years, rated the inten-
sity of NP as 4.22.0 (score out of 10), and scored
15.36.5 on the Neck Disability Index. Participants stood
on a moveable platform during which 32 randomized pos-
tural perturbations (eight repetitions of four perturbation
types: 8cm forward slide (FS), 8cm backward slides, 10
forward tilt, and 10 backward tilt) with varying inter-
perturbation time intervals were performed over a period
of 5min. Bilateral surface electromyography (EMG) from
the SCM and SC was recorded, and the onset time and
the average rectified value of the EMG signal was deter-
mined for epochs of 100ms; starting 100ms prior to and
500ms after the perturbation onset. Individuals with NP,
as compared to HC, demonstrated delayed onset times and
reduced EMG amplitude of the SCM and SC muscles in
response to all postural perturbations. Such findings were
S.A.Boudreau(*)
Department ofHealth Science andTechnology, Faculty
ofMedicine, Aalborg University, lborg, Denmark
e-mail: sboudreau@hst.aau.dk
D.Falla
Pain Clinic, Center forAnesthesiology, Emergency andIntensive
Care Medicine, University Hospital Gttingen, Gttingen,
Germany
D.Falla
Department ofNeurorehabilitation Engineering, Bernstein Focus
Neurotechnology Gttingen, Bernstein Center forComputational
Neuroscience, University Medical Center Gttingen,
Georg-August University, Gttingen, Germany
most pronounced following the FS postural perturbation
(healthy vs. NP for SCM 83.38.0 vs. 86.34.4 and SC
75.63.5 vs. 89.34.2), which was also associated with
the greatest change (expressed in % relative to baseline) in
EMG amplitude (healthy vs. NP for SCM 206.650.4 vs.
115.915.7 and SC 83.419.2 vs. 69.210.9) across
all postural perturbations types. Individuals with NP dis-
play altered neural control of the neck musculature in
response to rapid, unanticipated full body postural pertur-
bations. Although the relative timing of neck musculature
activity in individuals with NP appears to be intact, simul-
taneous co-activation of the neck musculature emerges for
unanticipated anteriorposterior postural perturbations.
Keywords Neck pain Perturbation Motor control
Balance Fall EMG
Introduction
The musculoskeletal system of the cervical spine is among
the most complex of the human body. The ability to rapidly
modulate the timing of neck muscles in response to unan-
ticipated postural perturbations is considered paramount for
maintaining and recovering balance. Under normal condi-
tions, automatic postural responses systematically vary
with the direction of an external perturbation in both onset
and amplitude (Moore etal. 1988; Rushmer etal. 1988;
Jones etal. 2008) and the activation profiles of the postural
muscles reflect the biomechanical demands imposed by
the postural perturbation (Falla etal. 2004; Thrasher etal.
2010; St-Onge etal. 2011).
Individuals with chronic neck pain (NP) demonstrate
poor balance for review see (Ruhe etal. 2011), as well as
reduced neck strength (Ylinen etal. 2004; Cagnie etal.
13

2012
2007; Scheuer and Friedrich 2010; Lindstrom etal. 2011),
and a loss of muscle specificity during the performance of
functional motor tasks (Falla etal. 2010; Lindstrom etal.
2011; Schomacher etal. 2012). In addition, individuals
with chronic NP display reduced and delayed onset of
neck muscle activity in response to anticipated postural
perturbations (Falla etal. 2004; Falla etal. 2011). In line
with these findings, individuals with chronic low back
pain (LBP) also demonstrate delayed and reduced elec-
tromyography (EMG) amplitude of trunk muscle activ-
ity compared with controls in response to anticipated
(Hodges 2001) as well as unanticipated (Magnusson etal.
1996; Radebold etal. 2000) postural perturbations. Taken
together, these studies suggest that feed-forward and auto-
matic motor control strategies are altered in a similar man-
ner in musculoskeletal pain conditions of the neck and low
back and have subsequently been the target of contem-
porary motor rehabilitation training regimes (Falla etal.
2013; Rittig-Rasmussen etal. 2013). However, whether
neck muscle activity is altered in response to unantici-
pated, full body perturbations in patients with chronic NP
remains unknown.
This study compares automatic postural responses of the
neck musculature to rapid, unanticipated, full body pertur-
bations in individuals with chronic NP and healthy controls
(HC). These functionally relevant postural perturbations
are produced by a computer-controlled platform that can
be maneuvered in three-dimensional space to produce tilt-
ing or sliding perturbations that resemble tripping over an
obstacle or slipping on a wet surface. The aim of the study
was to determine whether automatic postural responses of
the neck musculature in individuals with chronic NP, as
compared to HC, is systematically altered following rapid,
unanticipated, full body postural perturbations in anterior
posterior tilting and sliding translations of the support sur-
face. Therefore, the onset and amplitude of sternocleido-
mastoid (SCM) and splenius capitus (SC) muscle activity
were assessed with EMG in response to rapid tilting (toe up
and toe down) and sliding (forward and backward) transla-
tions of the support surface.
Methods
Participants
Individuals with a history of either chronic idiopathic- or
trauma-induced NP and age-matched HC participated in a
single experimental session. Patients were sought for the
study through referral from general practitioners or through
general advertising in the popular press and were consid-
ered for the study if they were suffering from persistent NP
and disability limiting their daily physical activity for at
13
Exp Brain Res (2014) 232:20112020
least 6months. Individuals with trauma-induced NP were
included if they reported a history (6months or longer)
of pain in the head, neck, or shoulder region originating
within 48h of a rear-end collision motor vehicle accident.
Patients with idiopathic NP were included if they had a his-
tory of insidious onset NP with or without headaches for a
minimum of 6months. Patients were excluded if they dis-
played the evidence of nerve root irritation. Healthy partici-
pants were included if they were free of NP and had no past
history of orthopedic disorders affecting the neck and no
history of neurological disorders.
A total of 16 HC (3 males) and 30 individuals with NP
(5 males) with a history of NP ranging from 6months to
30years participated. Seven individuals with NP reported
onset of pain in the head, neck, or shoulder region origi-
nating within 48h of a rear-end collision motor vehicle
accident.
All participants signed an informed consent form prior to
the experimental session. Ethics approval for the study was
granted by the regional Ethics Committee (N-20100083),
and the procedures were conducted according to the Decla-
ration of Helsinski.
Disability, pain history, andintensity
Participant demographics (age, weight, and height), history,
current symptoms, which included current and average
pain intensity over the last 4weeks (NRS, 0-10), and pain
duration (years) were recorded. Perceived pain and dis-
ability were also assessed using the Neck Disability Index
(NDI) (score 050) (Vernon and Mior 1991; Vernon 2008).
For all participants, current NP intensity was recorded on a
10-cm NRS anchored with no pain and the worst pos-
sible pain imaginable just prior to the onset of the postural
perturbations.
Postural perturbations
Postural perturbations were produced using a computer-
controlled movable platform as previously described
(Andersen and Sinkjaer 2003). Participants were instructed
to step onto the center of the platform and position their
feet, approximately, shoulder width apart such that they
were able to stand in a comfortable posture. The position
of the feet was then marked in the event the individual was
required to relocate their footing. Participants were asked
to focus on a target located ~3m from the platform. The
focus was used to facilitate similar starting posture between
the postural perturbations. Four different postural pertur-
bations were produced with varying inter-perturbation
time intervals (range 720s) in order to reduce the par-
ticipants ability to predict the type and perturbation onset.
The four postural perturbations, refer to Boudreau etal.

2012
2007; Scheuer and Friedrich 2010; Lindstrom etal. 2011),
and a loss of muscle specificity during the performance of
functional motor tasks (Falla etal. 2010; Lindstrom etal.
2011; Schomacher etal. 2012). In addition, individuals
with chronic NP display reduced and delayed onset of
neck muscle activity in response to anticipated postural
perturbations (Falla etal. 2004; Falla etal. 2011). In line
with these findings, individuals with chronic low back
pain (LBP) also demonstrate delayed and reduced elec-
tromyography (EMG) amplitude of trunk muscle activ-
ity compared with controls in response to anticipated
(Hodges 2001) as well as unanticipated (Magnusson etal.
1996; Radebold etal. 2000) postural perturbations. Taken
together, these studies suggest that feed-forward and auto-
matic motor control strategies are altered in a similar man-
ner in musculoskeletal pain conditions of the neck and low
back and have subsequently been the target of contem-
porary motor rehabilitation training regimes (Falla etal.
2013; Rittig-Rasmussen etal. 2013). However, whether
neck muscle activity is altered in response to unantici-
pated, full body perturbations in patients with chronic NP
remains unknown.
This study compares automatic postural responses of the
neck musculature to rapid, unanticipated, full body pertur-
bations in individuals with chronic NP and healthy controls
(HC). These functionally relevant postural perturbations
are produced by a computer-controlled platform that can
be maneuvered in three-dimensional space to produce tilt-
ing or sliding perturbations that resemble tripping over an
obstacle or slipping on a wet surface. The aim of the study
was to determine whether automatic postural responses of
the neck musculature in individuals with chronic NP, as
compared to HC, is systematically altered following rapid,
unanticipated, full body postural perturbations in anterior
posterior tilting and sliding translations of the support sur-
face. Therefore, the onset and amplitude of sternocleido-
mastoid (SCM) and splenius capitus (SC) muscle activity
were assessed with EMG in response to rapid tilting (toe up
and toe down) and sliding (forward and backward) transla-
tions of the support surface.
Methods
Participants
Individuals with a history of either chronic idiopathic- or
trauma-induced NP and age-matched HC participated in a
single experimental session. Patients were sought for the
study through referral from general practitioners or through
general advertising in the popular press and were consid-
ered for the study if they were suffering from persistent NP
and disability limiting their daily physical activity for at
13
Exp Brain Res (2014) 232:20112020
least 6months. Individuals with trauma-induced NP were
included if they reported a history (6months or longer)
of pain in the head, neck, or shoulder region originating
within 48h of a rear-end collision motor vehicle accident.
Patients with idiopathic NP were included if they had a his-
tory of insidious onset NP with or without headaches for a
minimum of 6months. Patients were excluded if they dis-
played the evidence of nerve root irritation. Healthy partici-
pants were included if they were free of NP and had no past
history of orthopedic disorders affecting the neck and no
history of neurological disorders.
A total of 16 HC (3 males) and 30 individuals with NP
(5 males) with a history of NP ranging from 6months to
30years participated. Seven individuals with NP reported
onset of pain in the head, neck, or shoulder region origi-
nating within 48h of a rear-end collision motor vehicle
accident.
All participants signed an informed consent form prior to
the experimental session. Ethics approval for the study was
granted by the regional Ethics Committee (N-20100083),
and the procedures were conducted according to the Decla-
ration of Helsinski.
Disability, pain history, andintensity
Participant demographics (age, weight, and height), history,
current symptoms, which included current and average
pain intensity over the last 4weeks (NRS, 0-10), and pain
duration (years) were recorded. Perceived pain and dis-
ability were also assessed using the Neck Disability Index
(NDI) (score 050) (Vernon and Mior 1991; Vernon 2008).
For all participants, current NP intensity was recorded on a
10-cm NRS anchored with no pain and the worst pos-
sible pain imaginable just prior to the onset of the postural
perturbations.
Postural perturbations
Postural perturbations were produced using a computer-
controlled movable platform as previously described
(Andersen and Sinkjaer 2003). Participants were instructed
to step onto the center of the platform and position their
feet, approximately, shoulder width apart such that they
were able to stand in a comfortable posture. The position
of the feet was then marked in the event the individual was
required to relocate their footing. Participants were asked
to focus on a target located ~3m from the platform. The
focus was used to facilitate similar starting posture between
the postural perturbations. Four different postural pertur-
bations were produced with varying inter-perturbation
time intervals (range 720s) in order to reduce the par-
ticipants ability to predict the type and perturbation onset.
The four postural perturbations, refer to Boudreau etal.
Exp Brain Res (2014) 232:20112020 2013
(2011), consisted of an 8-cm forward slide (FS), 8-cm
backward slide (BS), 10 forward tilt (FT), and backward
tilt (BT) of the platform around the middle axis in the fron-
tal plane. The platform had a constant velocity of 270cm/
ms and 120/ms from starting position (ground height and
level) to the end position for the slides and tilts, respec-
tively. Pilot trials revealed that these postural perturbation
parameters resulted in marked activity of the SCM and SC
muscles without producing discernible compensatory pos-
tural movements of the arms and legs. In each experimental
condition, all four perturbations were repeated 8 times in
random order for a total of 32 perturbations. After each per-
turbation, the platform slowly returned to the starting posi-
tion. The 32 perturbations were completed over a 45-min
interval. Prior to the onset of the experimental protocol, the
participants experienced each type of postural perturba-
tion in order to avoid the possibilities of startle responses
(Blouin etal. 2006) and dramatic attenuation in responses
from the first perturbation (Blouin etal. 2003). These pos-
tural perturbations were considered unanticipated since
any specific anticipation to a perturbation direction or type
would, conceivably, increase the risk of instability (Laven-
der etal. 1993).
Electromyography
Following skin preparation, bipolar surface EMG signals
were detected from the SCM and SC muscles bilaterally
with pairs of electrodes (Ambu Neuroline 720, Denmark)
positioned 20mm apart following guidelines for elec-
trode placement (Falla etal. 2002). A reference electrode
(Ambu Neuroline Ground, Denmark) was attached around
the right wrist. The EMG signals were sampled at 2,048Hz
with a gain of 2,000 using a 128-channel surface EMG-
USB amplifier (OT Bioelettronica, Torino, Italy; 3-dB
bandwidth 10500Hz) and converted to digital form by a
12-bit analog-to-digital converter.
Fig.1Representative EMG
activity for the right (R) and left
(L) SCM and SC relative to the
postural perturbation trigger
(dashed line) with labeled (open
triangle) EMG onset detection
A trigger signal originating from the computer-con-
trolled platform was used as a reference in order to deter-
mine the onset of SCM and SC muscle activity following
each postural perturbation. Similar to our previous inves-
tigation of activation patterns of the low back in response
to postural perturbations (Boudreau etal. 2011), the aver-
age rectified value (ARV) was estimated from the EMG
signals over non-overlapping signal epochs of 100ms.
The first 100-ms epoch was recorded prior to the pertur-
bation onset (100ms), and the remaining epochs were
recorded thereafter. The ARV of the EMG was assessed
over each 100ms until 500ms following the onset of the
perturbation. The ARV of the EMG epochs for each per-
turbation trial was averaged and normalized to baseline
(100 to 0ms) ARV for each participant. The change in
EMG amplitude of the SCM and SC following the postural
perturbations is expressed as the mean percent change in
the amplitude of the ARV over the interval 100500-ms
post-perturbation. The 100500-ms timeframe was chosen
in order to assess and contrast the change in SCM and SC
muscle activation in response to the postural perturbations.
Previously developed software for muscle activity detec-
tion from EMG signals was utilized to determine the onset
time of SCM and SC activity (for a complete description of
the algorithm used, refer to the work of Merlo etal. (2003).
This software is based on identifying single motor unit
action potentials from the interference EMG signal using
the continuous wavelet transform. A manifestation variable
is computed as the maximum of the outputs of a bank of
matched filters at different scales. A threshold is applied
to the manifestation variable to detect EMG activity. With
the method proposed by Merlo etal. (2003), the standard
deviation of onset estimate reduces from 26 to 17ms when
the signal to noise ratio varies from 2 to 8dB, while the
single threshold approach leads to a standard deviation of
onset estimate always >130ms and results in the worst per-
formance. Figure1 shows a representative example of the
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2014
onset detection, using the method proposed by Merlo etal.
(2003) relative to the postural perturbation trigger.
The mean onset time and EMG amplitude as determined
from the eight postural perturbations for each postural per-
turbation type was used for further statistical analysis.
Statistical analysis
The onset and EMG amplitude of the left and right SCM
and SC were first compared for differences between sides
using Students paired t test. No differences were found
between sides therefore the mean of the left and right
onset times and EMG amplitude for the SCM and SC were
pooled and used for further analyses.
A three-way ANOVA was first used to compare the onset
times and EMG amplitude of the SCM and SC between
individuals with NP and HC across the four perturbation
types (FS, BS, AT, and PT). Further analysis followed with
two-way repeated-measures (RM) ANOVA to assess dif-
ferences between the activation patterns (onset times and
change in amplitude) of the SCM and SC with respect to
perturbation type. A two-way RM ANOVA was then used
to assess the time course of SCM and SC muscle activity
for each perturbation type between individuals with NP and
HC with time (baseline; 0100; 100200; 300400; and
400500ms post-perturbation onset) as the repeated factor.
Significant differences revealed by ANOVA were followed
by post hoc StudentNewmanKeuls (SNK) test.
Pearsons correlations were used to further investigate sig-
nificant differences in the muscle activation patterns between
Table1Demographics and pain characteristics for the health controls (HC) and individuals with neck pain (NP)
Groups Age (years) Weight (kg) Height (cm)
HC 36.510.9 74.517.4 169.718.6
NP 35.610.0 69.313.3 173.19.6
Data are reported as meanSD
Fig.2Onset times of the a
SCM and b SC activity for
healthy controls (HC) and
individuals with chronic neck
pain (NP) across the four dif-
ferent postural perturbations
(FS forward slide, BS backward
slide, FT forward tilt, and BT
backward Tilt)
13
Exp Brain Res (2014) 232:20112020
individuals with NP and HC across the postural perturba-
tions. Correlation results are reported together with a Bon-
forreni test for multiple comparisons. Results are reported
as mean and standard error (SE) in text and figures, unless
stated otherwise. Statistical significance was set at P<0.05.
Results
Participants
There were no differences between age, weight, and height
between the groups (P>0.5), as can be viewed in Table1,
together with current pain, NDI, and pain duration charac-
teristics of the NP group. Prior to the onset of the experi-
mental session, individuals with NP rated their current pain
(meanSD) as 3.61.9 out of 10 (NRS).
Muscle onset times
All participants were able to regain posture and balance
following the unanticipated postural perturbations. As
shown in Fig.2, the SCM and SC onset times were delayed
for individuals with NP in comparison with HC (three-way
ANOVA, F=5.2, P=0.024, post hoc SNK, P=0.023),
but the relative timing between the onset times across per-
turbation types was maintained in the patients with NP
(three-way ANOVA, F=0.6, P=0.561).
For both HC and individuals with NP, the onset times of
the SCM did not vary across perturbation types (two-way
Average pain NDI Pain duration (years)
4.22.0 15.36.5 8.97.8
Exp Brain Res (2014) 232:20112020 2015
Fig.3Increases in EMG amplitude relative to baseline for the a SCM and b SC activity for healthy controls (HC) and individuals with chronic
neck pain (NP) across the four different postural perturbations (FS forward slide, BS backward slide, FT forward tilt, and BT backward Tilt)
RM ANOVA, F =0.397, P =0.75). However, the onset
times of the SC occurred later (two-way RM ANOVA,
F=4.96, P=0.003) following the BS in comparison with
the FS (post hoc, P<0.001), FT (post hoc, P=0.004), and
BT (post hoc, P =0.004). For both HC and individuals
with NP, the onset time of the SCM was earlier than the SC
(two-way RM ANOVA, F =13.1, P<0.001) for the BS
(post hoc, P=0.002) and BT (post hoc, P=0.002) with a
mean difference of 10.96ms.
Muscle activation
Regardless of the postural perturbation type (three-way
ANOVA, F =1.471, P =0.22), a main finding was that
the change in amplitude of SCM and SC muscle activity in
response to the postural perturbations was lower for indi-
viduals with NP as compared to HC (three-way ANOVA,
F =6.7, P =0.01, post hoc SNK, P<0.009; refer to
Fig.3), but a reduction in amplitude of the SCM as com-
pared to the SC muscle activity could not be shown (three-
way ANOVA, F=3.33, P=0.07).
For both individuals with NP and HC, the change in the
amplitude of SCM was more pronounced than SC (three-way
ANOVA, F=3.79, P=0.011) but only in response to the FS
(post hoc SNK, P<0.001). Further, SCM muscle activity was
greater in response to the FS as compared to the other pos-
tural perturbations, that is the BS, FT, and BT (two-way RM
ANOVA, F =16.6, P<0.001; post hoc SNK, P<0.001).
The SC muscle activity also co-varied in response to the pos-
tural perturbation type (two-way RM ANOVA, F =19.26,
P<0.001), showing greater activation for the FS and BS in
comparison with the FT and BT (post hoc, P<0.01).
Time course ofmuscle activity
The time course of SCM and SC activation profiles for
individuals with NP and HC is shown for each postural
perturbation in Fig.4. Differences between individuals
with NP and HC were most evident for the FS postural
perturbation.
Forward slide (FS)
The time course of SCM activity differed between HC
and individuals with NP (two-way RM ANOVA, F=3.5,
P=0.009). For HC, the activation of the SCM significantly
increased 300ms following the postural perturbation (post
hoc SNK, P<0.001), but no change could be shown for
individuals with NP (post hoc SNK, P>0.37). For HC and
individuals with NP, the time course of SC activity varied
following the perturbation onset (two-way RM ANOVA,
F=19.9, P<0.001) with increased activation at 300ms
following the perturbation onset (post hoc SNK, P<0.001)
and no change thereafter (post hoc SNK, P>0.05).
Backward slide (BS)
For both the HC and individuals with NP, the time course of
SCM activity varied following the perturbation onset (two-
way RM ANOVA, F =10.9, P<0.001) with increased
activation at 200ms following the perturbation onset (post
hoc SNK, P<0.001) and no change thereafter (post hoc
SNK, P>0.05). The time course of SC activity also varied
following the perturbation onset (two-way RM ANOVA,
F=24.0, P<0.001), but with increased activation occur-
ring at 300ms following the perturbation onset (post hoc
SNK, P<0.001) and no change thereafter (post hoc SNK,
P>0.05).
Forward tilt (FT)
For HC and individuals with NP, the time course of SCM
activity varied following the perturbation onset (two-
way RM ANOVA, F =10.8, P =0.004) with increased
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Fig.4Time course of SCM and SC activity, relative to baseline, for healthy controls (HC) and individuals with chronic neck pain (NP) follow-
ing a FS, b BS, c FT, and d BT postural perturbations
activation at 300ms following the perturbation onset (post
hoc SNK, P =0.004) and no change thereafter (post hoc
SNK, P>0.05). For HC and individuals with NP, the acti-
vation of the SC muscle varied following the perturbation
onset (two-way RM ANOVA, F=2.5, P=0.045), but no
change at any particular time point could be shown (post
hoc SNK, P>0.8).
Backward tilt (BT)
The time course of SCM activity was similar between HC
and individuals with NP (two-way RM ANOVA, F=11.1,
P<0.001) with increased activation at 300ms follow-
ing the perturbation onset (post hoc SNK, P=0.003) and
no change thereafter (post hoc SNK, P>0.05). The time
course of SC activity was also similar between HC and
individuals with NP (two-way RM ANOVA, F =11.7,
P=0.004), but with increased activation at 300ms follow-
ing the perturbation onset (post hoc SNK, P<0.001) and
no change thereafter (post hoc SNK, P>0.05).
Onset timesand muscle activity correlations
A consistent finding for both groups was that the EMG
amplitudes of the SCM and SC were highly correlated for
all postural perturbations (Pearsons correlation, P<0.005,
13
Exp Brain Res (2014) 232:20112020
Bonforreni correction P<0.05, refer to Fig.5ad). There
were no correlations between the EMG amplitude and
onset time for either muscle in either group (Pearsons cor-
relation, P>0.05). However, the onset times of the SCM
and SC were correlated for the FS perturbation for individ-
uals with NP (Pearsons correlation, P=0.040, with Bon-
forreni correction P>0.05, refer to Fig.6).
Discussion
The present study examined postural responses of the SCM
and SC muscles in healthy and NP patient populations in
response to rapid, unanticipated full body perturbations.
A key finding of this study was the reduced activation and
delayed onset times of the SCM and SC muscles for indi-
viduals with chronic NP as compared to HC across all four
perturbation types. Such differences were most pronounced
following the FS postural perturbation, which was associ-
ated with the greatest neck muscle activity across the per-
turbations types. The time course of SCM and SC activa-
tion was similar for individuals with chronic NP and HC
with the exception of the FS. Indeed, the activation pro-
files of the SCM and SC co-varied in response to the pos-
tural perturbation type, but the greatest changes in activa-
tion of these muscles occurred for the FS and BS. Strong
Exp Brain Res (2014) 232:20112020 2017

Fig.5Correlated increases SCM and SC EMG amplitudes, relative to baseline, for healthy controls (HC) and individuals with chronic neck
pain (NP) (P<0.005) following a FS, b BS, c FT, and d BT postural perturbations

Fig.6Onset times of the SCM and SC for a the healthy controls response to the FS postural perturbation. Onset times of the SCM
(HC) and b individuals with chronic neck pain (NP) showing cor- were stratified to illustrate the differences in the activation profiles
related onset times between the SCM and SC for the NP group in between the HC and NP groups

correlations were found between the change in SCM and
SC muscle activity for both individuals with chronic NP
and HC in response to the postural perturbations. An inter-
esting finding was that the onset times of the SCM and SC
were generally uncorrelated; however, the evidence for
correlated onsets following the FS postural perturbation
emerged for individuals with NP. Overall, this study pro-
vides novel insight into the postural responses of selected
neck muscles in response to rapid, unanticipated full body
perturbations and corroborates evidence for impaired neu-
ral control of the neck muscles in individuals with chronic
NP.
Previously it has been shown that when a perturbation
to the spine occurs, such as during a rapid arm movement,
onset of the neck flexor muscles is delayed in people with
NP (Falla etal. 2011, 2004). The delay in onset of these
muscles exceeds the criteria for feed-forward contraction
during movements, which indicates a significant deficit in

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the automatic feed-forward control of the cervical spine. An
additional observation in people with NP is that the activa-
tion of the deep cervical flexor muscles adopts a direction-
specific response, which is in contrast to that observed
in healthy individuals (Falla etal. 2004). Until now, the
knowledge on postural responses of neck muscles to pertur-
bations in patients with NP has been limited to anticipated,
internal perturbations. This study examined, for the first
time, postural responses in patients with NP to fast, func-
tionally relevant, full body perturbations. The onset times
of both the SCM and SC muscles were delayed in individu-
als with chronic NP, as compared to HC, in response to the
unanticipated full body perturbations. The delay in neck
muscle activation in response to either anticipated or an
unanticipated postural perturbation is likely to impact the
control and stability of the head and cervical spine.
The onset times of the SCM and SC, in healthy individu-
als, occur comparably later than those we have previously
found for the erector spinae and external oblique using the
same perturbation protocol (Boudreau etal. 2011), suggest-
ing that the response of the neck musculature could be sub-
ject to feed-forward control initiated from more distal pos-
tural control muscles, i.e., the trunk or anticipatory postural
adjustments (APAs). Presumably, the postural response
of the cervical musculature must account and/or antici-
pate the displacement of the center of mass of the lower
trunk, which can also be viewed as an additional source of
head perturbation (Aruin etal. 1998). In conditions where
demands for stability are high, APAs are attenuated (Aruin
etal. 1998). The perceived demands for postural stability
in individuals with chronic NP likely differed from their
healthy equivalents in the present study, as there is ample
evidence to support that standing balance is impaired;
especially in the anteriorposterior directions for review
see (Ruhe etal. 2011). Therefore, increased APAs are an
unlikely source of the reduced and delayed activation of the
neck muscles for individuals with chronic NP in response
to unanticipated postural perturbations.
The present finding that the activation of the SCM mus-
cle was more pronounced than SC muscle is consistent
with the relationship between EMG activity and isometric
assessments of neck muscle strength (Kumar etal. 2002;
Gabriel etal. 2004). Greater EMG activity is expected to
occur in flexion than extension for a given force, and more
prominent muscle activation of the neck and trunk has been
shown in response to forward perturbations in comparison
with backward perturbations during sitting (St-Onge etal.
2011). Of the postural perturbations employed in the pre-
sent study, only the SCM is being recruited in directions
by which this muscle group is either strongest (flexion) or
weakest (extension) (Kumar etal. 2002). The SCM muscles
are considered as head and neck long flexor muscles when
bilaterally contracted. However, during head and neck
13
Exp Brain Res (2014) 232:20112020
extension, the SCM muscles provide a proper line of action
to extend the craniocervical joint and this may explain the
relatively prominent activation patterns of the SCM mus-
cle, as compared to the SC muscle, across all postural per-
turbation types and directions.
In healthy subjects, neck muscles show well-defined
preferred directions of activation during multidirectional
isometric contractions, which are in accordance with their
anatomical position relative to the spine. For example,
under healthy conditions, SC muscle activity is most domi-
nant during lateral and posterolateral extension (Kumar
etal. 2002; Gabriel etal. 2004; Falla etal. 2010). However,
recent studies have shown that patients with either whip-
lash-induced NP or idiopathic NP have reduced specificity
of neck muscle activity and increased co-activation of neck
muscles with respect to asymptomatic individuals (Falla
etal. 2010; Lindstrom etal. 2011; Schomacher etal. 2012).
The present study found that the change in SCM and SC
muscle activity, in both individuals with NP and HC, was
highly correlated, suggesting that a scaled response via a
common drive to these muscles may be present in response
to rapid, unanticipated full body perturbations. However, in
response to the FS postural perturbation, which can be con-
sidered as the perturbation with the highest postural threat,
individuals with chronic NP showed correlated onsets
times of the SCM and SC. In contrast, healthy individu-
als demonstrated variable onset times of the SC muscle,
and moreover, depending on the SC onset time, activation
of the SCM muscle occurred either before or after. Under
healthy conditions, the present results provide evidence for
reciprocal activations of the SCM and SC, during the FS,
and this likely reflects the expected variation of possible
response profiles within a normal population of individu-
als with intact neural control of the neck muscles. In con-
trast, for those individuals with NP, the onset time of the
SCM and SC was positively correlated and such findings
extend to the notion that the ability to appropriately and
independently recruit the cervical musculature to match the
demands of the motor task (postural perturbation) is lost.
Moreover, individuals with NP appear to respond in a simi-
lar way to an unanticipated postural response. These find-
ings, however, should be followed up in a subsequent inves-
tigation as these specific findings were, in part, exploratory
and multiple correlations were made.
Limitations
A larger sample size in this study could have enabled the
use of clustering techniques to identify whether there is a
clear subset of individuals with chronic NP who demon-
strate altered neural control of the neck musculature. Fur-
thermore expanding the postural perturbation protocol to
include FS and BS (anteriorposterior) perturbations of
Exp Brain Res (2014) 232:20112020 2019
differing magnitude and/or acceleration would provide
more clear evidence whether individuals with chronic
NP can appropriately match postural demands. In healthy
individuals, SCM onset latency appears to decrease as the
severity of the perturbation increases (Brault etal. 1998);
more specifically, latencies in an 8-kph rear-end impact are
12ms shorter than those in 4-kph impacts, as assessed in a
seated position. Whether such relations are maintained in
individuals with NP remains unknown.
Perspectives
The findings of this study suggest that individuals with
NP may be at risk of further injury when an unanticipated
postural perturbation that displaces the head and neck in a
whiplash-like motion, as induced in the FS postural pertur-
bation, occurs. Development of a fundamental movement
test suitable for clinical practice, which aims to assess the
response profile of the head and neck to an unanticipated
postural perturbation, would provide insight into the risk
and possibly the extent of reduced neural control of the
neck muscles. To date, no such clinical assessment exists.
Conclusions
This present study provides evidence for altered neural
control of the neck musculature in individuals with chronic
NP in response to rapid, unanticipated full body postural
perturbations. The results indicate that the neck muscula-
ture systematically responds to variations imposed by the
postural perturbations, but the amplitudes and onset of neck
muscle activation are reduced and delayed in NP. The rela-
tive timing of neck musculature activity in individuals with
NP appears to be intact, but simultaneous co-activation of
the neck musculature emerges for unanticipated anterior
posterior postural perturbations.
AcknowledgmentsThis study was co-financed by Redcord AS,
Norway and Aalborg University, Denmark.
Conflict of interestThe authors do not have conflicts of interest.
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