J Appl Physiol 99: 141153, 2005.
First published October 15, 2004; doi:10.1152/japplphysiol.00494.2004.
Neck muscle fatigue and spatial orientation during stepping in place
in humans
Micaela Schmid1 and Marco Schieppati1,2
1
Human Movement Laboratory, Centro Studi Attivita` Motorie, Fondazione Salvatore Maugeri, Scientific Institute of
Pavia, and 2Department of Experimental Medicine, Section of Human Physiology, University of Pavia, Pavia, Italy
Submitted 10 May 2004; accepted in final form 10 August 2004
Schmid, Micaela, and Marco Schieppati. Neck muscle fatigue
and spatial orientation during stepping in place in humans. J Appl
Physiol 99: 141153, 2005. First published October 15, 2004;
doi:10.1152/japplphysiol.00494.2004.Neck proprioceptive input,
as elicited by muscle vibration, can produce destabilizing effects on
stance and locomotion. Neck muscle fatigue produces destabilizing
effects on stance, too. Our aim was to assess whether neck muscle
fatigue can also perturb the orientation in space during a walking task.
Direction and amplitude of the path covered during stepping in place
were measured in 10 blindfolded subjects, who performed five 30-s
stepping trials before and after a 5-min period of isometric dorsal neck
muscle contraction against a load. Neck muscle electromyogram
amplitude and median frequency during the head extensor effort were
used to compute a fatigue index. Head and body kinematics were
recorded by an optoelectronic system, and stepping cadence was
measured by sensorized insoles. Before the contraction period, sub-
jects normally stepped on the spot or drifted forward. After contrac-
tion, some subjects reproduced the same behavior, whereas others
reduced their forward progression or even stepped backward. The
former subjects showed minimal signs of fatigue and the latter ones
marked signs of fatigue, as quantified by the dorsal neck electromyo-
gram index. Head position and cadence were unaffected in either
group of subjects. We argue that the abnormal fatigue-induced affer-
ent input originating in the receptors transducing the neck muscle
metabolic state can modulate the egocentric spatial reference frame.
Notably, the effects of neck muscle fatigue on orientation are opposite
to those produced by neck proprioception. The neck represents a
complex source of inputs capable of modifying our orientation in
space during a locomotor task.
locomotion; reference frame
AN IMPRESSIVE NUMBER OF PAPERS have recently appeared about
the multifarious roles of the neck muscle proprioceptive input
on the perception of body segment position and body orienta-
tion in space. A clear example of the relevance of neck input
for the subjects reference frame comes from studies of neck
vibration after cortical lesions leading to neglect of the con-
tralateral space and/or body. These studies clearly show that
neck vibratory treatment improves neglect symptomatology.
This clear superiority over other treatments might result from
the partial (re)activation of a distributed, multisensory network
in the lesioned hemisphere (Ref. 36; for a review, see Ref. 39)
that is triggered by the spindle afferent input activated by the
vibration. Most likely, the parietal cortex plays a role in the
egocentric representation of space and its calibration, since
many of its areas receive signals from the neck muscles and the
labyrinth (2).
Address for reprint requests and other correspondence: M. Schieppati,
Centro Studi Attivita` Motorie (CSAM), Fondazione Salvatore Maugeri
(IRCCS), Istituto Scientifico di Pavia, Via Ferrata 8, I-27100 Pavia, Italy
(E-mail: mschieppati@fsm.it).
http://www. jap.org 8750-7587/05 $8.00 Copyright 2005 the American Physiological Society
Less amazing, but certainly nonnegligible, effects can be
produced by neck muscle vibration in normal subjects, in
particular on body segment orientation and body sway during
quiet stance and on walking features. In standing subjects, neck
muscle vibration induces body tilt and increases sway, sug-
gesting that posture is organized with respect to a body
schema, to the construction of which the spindle input from
the neck contributes together with eye and skeletal muscle (15,
23, 32, 38, 44, 54, 55). During stepping in place, bilateral
vibration of the dorsal neck muscles produces an involuntary
forward stepping without modifying the stepping frequency
and in treadmill locomotion produces an involuntary steplike
increase of walking speed (33). One-sided lateral neck muscle
vibration, in the absence of vision, produces deviation of the
trajectory during normal walking (3) and body rotation during
stepping in place (4); under both conditions, the deviation is
opposite to the vibrated site. On a different vein, Goodwin et
al. (20) originally described proprioceptive illusions induced
by muscle vibration. It was later shown that neck muscle
vibration also elicits apparent motion of a stationary visual
target and deviation of the perceived straight ahead, possibly
by producing a change in the egocentric body-centered coor-
dinate system (1, 37, 62).
Muscle vibration is certainly an artificial situation, with its
major advantage being the good selectivity of its effects on the
muscle spindles primary terminations (11). Are there natu-
ral stimuli able to elicit similar effects, e.g., changes in length
of the neck muscles connected with head posture? Head and
eyes systematically deviate toward the future direction of the
curved trajectory (21), suggesting an anticipatory role of the
neck muscle for body steering while walking. Body sway
increases when subjects stand with their heads turned or
extended and their eyes closed (5, 58). Early observations
suggested that cervical proprioceptive input could affect the
direction of body sway by acting on the central vestibular
system (28). More recently, it has been shown that neck input
has an influence on the direction of body displacement induced
by galvanic vestibular stimulation (18). Moreover, natural
proprioceptive stimulation (head rotation) affects the percep-
tion of the head position, object localization, and movement in
the visual space (46, 48). It has also been shown that vestibu-
lar-proprioceptive interactions play a role in self-motion per-
ception in addition to postural control (47).
On the other hand, disturbances of the neck musculature
could bring about dizziness or unsteadiness, the so-called
cervicogenic dizziness (6). A report by Schieppati et al. (56)
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141
142 NECK MUSCLE FATIGUE AND STEPPING IN PLACE
showed that prolonged contraction of dorsal neck muscles,
bilaterally, can alter balance control through a mechanism
connected to fatigue-induced afferent inflow. Strong and pro-
longed neck muscle contractions have also been recently
shown to produce postural responses (14). Fatigue-related
sensory input may be the result of an increased outflow from
the free nerve endings as a consequence of ionic or metabolic
changes (elevated interstitial potassium concentration or insuf-
ficient oxygen availability due to reduced blood flow) (19, 52).
Muscle fatigue can indeed affect joint position sense (Refs. 12,
57, 60; for a recent review, see Ref. 63), and abnormal cervical
pain-related input is able to significantly alter postural control
(35).
In this study, we have tested the hypothesis that dorsal neck
muscle fatigue could affect the reference system for the orien-
tation of body position in space. In particular, the effects of a
fatiguing contraction have been tested on the capacity of
stepping in place. This task reproduces several features of
normal walking (8), such as the cyclic single-leg support of the
body and the need for accurate control of balance. It can also
be more easily captured by a movement-analysis system for
extended periods of time than by normal locomotion. As such,
this task should be at least as sensitive as normal floor walking
to possible disorientation-producing stimuli. Perhaps, it could
be even more sensible than normal walking, because, contrary
to the latter, it lacks the advantage given by the kinetic energy
of the body progressing in one direction. The stepping-in-place
task has been previously employed as a test for vestibular
deficits and balance problems, even if its reliability in this
context has been repeatedly challenged (50). Because the
isometric contraction of the dorsal neck muscles was bilateral
and symmetrical, we assumed that postcontraction changes in
the body position during the stepping-in-place test could be
detected along the subjects sagittal plane, much like it oc-
curred as a consequence of bilateral dorsal neck muscle vibra-
tion, which induced an increased velocity in the stepping
progression along the straight-ahead direction (32).
METHODS
Subjects. Ten healthy subjects (9 men and 1 women, mean age 26.2
yr, range 2233 yr) volunteered to participate. No subject had a
history of neck pain or cervical column disease or had suffered head
trauma or whiplash injury. Informed consent was obtained according
to the Declaration of Helsinki. The local Ethics Committee approved
the investigation and experimental procedures.
Procedures. Subjects were asked to step in place at a self-selected
pace, blindfolded in a dim-lighted room. Before the start of the
acquisition session, subjects were free to step in place with eyes open
to feel confident with the maneuver. Then four blocks of stepping
trials were acquired, each composed of five successive trials. Each
trial lasted 30 s. After each trial, the subjects were repositioned at the
starting point by one experimenter before the next trial began. It was
checked that, at the beginning of each trial, the subjects started from
the same initial standing position, with the orientation of feet, trunk,
and head aligned. The starting signal was given by the experimenter
after a verbal warning signal. The four blocks were the control,
postcontraction 1, recovery, and postcontraction 2 blocks. After the
control and recovery blocks, subjects performed a 5-min-long tonic
isometric bilateral contraction of the dorsal neck muscles against a
load (see Isometric contraction of dorsal neck muscles) while standing
on the starting spot. At the end of this period, subjects immediately
started the first trial of the postcontraction (1 or 2) block. A rest period
J Appl Physiol VOL
of !30 min separated the postcontraction 1 block from the recovery
block. The subjects preparation with the markers and electrodes took
!30 min. The entire stepping session lasted !1 h. The same subjects
have also been recruited in an additional session, in a different day,
when they were asked to step in place and again perform four blocks
of five subsequent stepping trials each, but without tonic isometric
contraction of the dorsal neck muscles (no-load session). This proce-
dure was performed as a control experiment to check that the repeti-
tion of the stepping trials per se produced no effect on body displace-
ment and to help in interpreting highly variable data.
Isometric contraction of dorsal neck muscles. A large belt was
passed around the head just above the ears, and a cable was fixed to
it frontally and medially in correspondence with the forehead. The
cable passed through a pulley fixed at a 1-m distance at head height.
The pulley was part of a versatile gym training column placed in front
of the subject. Its vertical position was adjustable so that the line of the
pulling action was horizontal. The other end of the cable was fixed to
an adjustable mass. The thorax of the subject leaned against a padded
vertical support firmly fixed to the cable column so that the action of
the mass did not displace the trunk and overall body posture. No
contraction of the body extensor muscle chain below the support level
was required, since there was no need to push the trunk or whole body
backward, owing to the thorax support, which nullified the body
forward-pulling action of the mass. Therefore, the muscle action was
broadly limited to the neck extensors, and the subject counteracted the
head-flexor torque exerted by the mass by contracting the dorsal neck
muscles. The subjects had visual feedback of the head position by way
of a target fixed to the cable, which had to remain coplanar with a
reference fixed to the column. This was sufficient enough to ensure
negligible head pitch during the head extensor effort against the
head-flexor torque produced by the mass. For each subject, the mass
was chosen so that it represented about one-third of the maximal
voluntary contraction (MVC; 25.5 " 8.5 kg), i.e., 9.5 " 2.0 kg, equal
to 34.9 " 9.5% of MVC. MVC was the highest force value exerted
during a 10-s period of neck extension, during which the subject was
encouraged to produce the strongest possible effort. This was mea-
sured by means of a mechanical dynamometer placed in series
between the head belt and the pulley. During the fatiguing periods, the
subject had to counteract the applied mass for 5 min. At the end of this
period, the mass and the padded support were quickly disconnected
and removed.
Electromyogram recording and processing. Electrical activity of
the dorsal neck (splenius) and ventral neck (sternocleidomastoid)
muscles (from both right and left side) was recorded using bipolar
prejelled surface electrodes, with a longitudinal distance of 1 cm
between the recording spots. The electrode pairs were placed on the
bellies of the dorsal neck muscles, 2 cm from the midline and 4 cm
below the cranial insertion, and on the belly of the sternocleidomas-
toid, about halfway from its proximal and distal insertion points. The
electrodes were left in place during the entire recording session. The
signals were differentially amplified (#1,000), filtered (cutoff fre-
quency of 500 Hz), and acquired at a sampling frequency of 1 kHz.
Data were recorded by the Telemg Multichannel Electromyograph
System (Bioengineering Technology Systems). The signals were
acquired for the initial 10-s period of each minute of the 5-min
contraction period. The analysis of the electromyogram (EMG) was
performed with the Acknowledge software (Biopac), and the EMG
amplitude (AMP) of the filtered and integrated signal and the signals
median power frequency (MF) were calculated over the recorded
epochs (49). The EMG activity plots of the splenius and sternoclei-
domastoid muscles, during the 10 s of minute 1 and the 10 s of minute
5, are shown in Fig. 1.
Procedure of quantification of muscle fatigue based on EMG
signal. Based on the changes in the AMP and MF between the
beginning and end of the contracting period, an EMG index of fatigue
was calculated for each subject using the following formula: index of
fatigue $ ratio of AMP/ratio of MF, where the ratio of AMP $ (AMP
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 NECK MUSCLE FATIGUE AND STEPPING IN PLACE 143

Fig. 1. Examples of traces of surface electromyogram (EMG), recorded from a dorsal [splenius (SPL), left] and anterior [sternocleidomastoid (SCM), right] neck
muscle in one subject. The raw traces have been recorded during the first (top) and last minute (bottom) of the 5-min tonic isometric bilateral contraction of the
dorsal neck muscles against a load. The selectivity of the contraction is witnessed by the silence of the anterior flexor muscle (SCM, right), both at the beginning
and the end of the contraction period. The development of fatigue is accompanied by an increase in amplitude of the SPL EMG from the first to the last minute
of contraction (compare top and bottom) and by a shift toward lower frequency values of the median frequency (MDF) in the power spectrum of the EMG
(middle) observed at minute 5 of contraction.

of the 10-s period of minute 5/AMP of the 10-s period of minute 1)
and the ratio of MF $ (MF of the 10-s period of minute 5/MF of the
10-s perod of minute 1).
This index is influenced by two variables that are known to be
affected by the fatigue phenomenon (49). To check that both variables
were influenced by fatigue in the present population, we plotted the
EMG median frequency vs. amplitude for each subject and for each
minute of the 5-min period of tonic contraction. Figure 2A shows four
examples of these relationships and the best-fit line for each of them.
In two cases, when the median frequency decreased, the amplitude
increased. In the other two cases, the best-fit line was less steep or flat.
The angular coefficients of the best-fit lines were thus calculated for
each subject and plotted against the corresponding indexes of fatigue.
In Fig. 2B, the result of this procedure is reported. The strong linearity
of this scatter [y $ %3.56x & 3.66; r2 $ 0.91; F(1,8) $ 87.035; P $
0.00001] is in favor of the appropriateness of the use of an index that
combines both EMG variables.
Cluster analysis (K means) was performed on the EMG data of all
subjects by including in the analysis both amplitude and median
frequency changes, with each being computed as the ratio of the last
and first minute of tonic contraction. When n $ 2 clusters were
imposed to the algorithm, the analysis divided the subjects into two
equal-size groups. It turned out that the two groups had values smaller
or larger than 1.5. For simplicity, we will label the groups as fatigue
and no-fatigue groups, respectively, even if the range of the indexes of
the latter group is from 0.98 and 1.45, meaning that some subjects of
this group showed minimal EMG signs of fatigue.
For each group, intermediate indexes of fatigue were also calcu-
lated by means of the above formula for the successive minutes, where
the minute 5 data were sequentially changed with the data of minutes
2, 3, and 4. Figure 3A reports the results for the fatigue group, and Fig.
3B reports results for the no-fatigue group. It can be appreciated that,
in the former group, the intermediate EMG indexes of fatigue mono-
tonically increased from the first to the last minute of the contraction
period, whereas the same indexes remained stationary in the latter
group.
To further validate the EMG index of fatigue against an indepen-
dent measure of fatigue, we measured the MVC of the dorsal neck

Fig. 2. A: EMG amplitude vs. EMG median

frequency for each successive minute of the
5-min period of tonic contraction. These re-
lationships are shown for 4 subjects, and the
best-fit line for each of them is plotted. For 2
subjects (solid symbols), when the median
frequency decreased, the amplitude in-
creased. For the other subjects (open sym-
bols), the best-fit line was less steep or flat. B:
angular coefficients of the best-fit lines cal-
culated for all subjects are plotted against the
corresponding indexes of fatigue. For A and
B, the equations of the best-fit lines are re-
ported.

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144 NECK MUSCLE FATIGUE AND STEPPING IN PLACE
Fig. 3. Indexes of fatigue calculated from the EMG variables (amplitude and
median frequency) for each successive minute of the isometric neck muscle
contraction. The mean indexes are reported for the subjects showing (A) and
not showing (B) signs of fatigue. It can be seen that, in the former group, there
was a progressive increase in the index values during the contraction period.
The same mean indexes remained stationary in the latter group.
muscles before and after the tonic contraction period. Then, we
plotted the value of MVC after the tonic contraction (as percentage) of
the initial MVC) against the EMG fatigue index. To this aim, 7 of the
10 subjects performed the two MVCs on a different day, the former
before and the latter immediately after a 5-min period of dorsal neck
tonic isometric contraction, against the same load they sustained in the
first experimental session. On average, the MVC recorded during the
former trial was not different from that measured during the first
experimental session (n $ 7; MVC $ 26.4 " 5.9 kg). Because three
of the original subjects could not participate in this evaluation, to
strengthen the validation procedure we increased the population by
recruiting six additional subjects (n $ 6; MVC $ 28.1 " 2.4 kg).
These subjects were subjected to the same procedure for measurement
of MVC and EMG as the original subjects, and the load was chosen
to be in the same range (11.3 " 1.4 kg). Figure 4 shows that the
percent drop in MVC induced by the tonic contraction significantly
increased [y $ %0.12x & 1.08; r2 $ 0.43; F(1,11) $ 8, 16; P $
0.015] with the increase in the EMG fatigue index.
The index was then used for further analysis of the fatigue effects
on stepping behavior, assuming that changes in the EMG index
correlated with peripheral fatigue (29).
Kinematic recording and processing. Body movement was re-
corded by the ELITE System (Bioengineering Technology and Sys-
tems) with eight infrared cameras. The reflective spherical markers
were attached to the skin on the right and left anterior-superior iliac
spine and to an adjustable helmet in these following positions: vertex
of the head, forehead (the central point between the two temples), and
lateral left and lateral right positions (the left and right temples,
respectively). The helmet was removed during the fatiguing procedure
and then repositioned, always in the same position, during the step-
ping trials. Before the helmet was removed, a sign of its position was
made on the skin.
The markers positions were sampled at a frequency of 100 Hz. The
body movement was obtained by computing the midpoint (average of
the coordinates) between the left and the right anterior-superior iliac
spine marker positions. The resulting point, which was labeled body
J Appl Physiol VOL
midpoint, could be considered a good approximation of the displace-
ments of the center of mass. In the working space, subjects were
positioned at the starting point with their mediolateral (M-L) body
axis along the working space x-axis and their anteroposterior (A-P)
body along the y-axis. Figure 5A shows an example of body midpoint
path in the working field during a stepping-in-place trial. The x values
of the body midpoint path vs. time and the y values vs. time were fitted
with a polynomial function, the order of which minimized the mean
squared error (Fig. 5B). In most cases, the algorithm chose a 10th-
order polynomial as the best fit. By plotting the x vs. y interpolating
polynomials, we obtained the interpolated path. In Fig. 5A, this is
superimposed on the acquired body midpoint path. The mean squared
errors have been taken as a measure of the body midpoint sway (in the
x- and y-axes) around the main direction of displacement. The dis-
placement of the subjects in the working space was quantified by the
A-P and the M-L displacement of the body midpoint on the x-y plane.
A-P displacements were calculated as the differences between the y
coordinates of the body midpoint at the starting point and at the final
point, whereas the M-L displacements were the differences between
the x coordinates of the same points.
To compare the postcontraction displacement changes across the
subjects despite the possible different directions (forward or back-
ward) of the postcontraction paths, an A-P index of displacement was
calculated. For each subject, it was defined as the A-P displacement of
the first trial of the first postcontraction trial (postcontraction 1) minus
the mean value of the A-P displacement of the control trials, divided
by the sum of the absolute values of these two numbers. This
procedure weights the differences against the absolute magnitude of
the traveled paths. A positive sign of the index meant A-P forward
displacement, and a negative sign meant A-P backward displacement.
Head movements were computed on the basis of the angle between
the line joining the helmet vertex to the helmet frontal marker and the
vertical axis versor (head pitch), and on the basis of the angle between
the line joining the helmet lateral right marker to the helmet lateral left
marker and the vertical axis versor (head roll).
Cadence recording. The cadence was recorded by the PedarMobile
Insole System (Novel, Munchen, Germany). The analog signal pro-
vided by the insole sensors was sampled at a frequency of 50 Hz, and
the data were stored in the memory card to leave a subject free to
move without cable constraints. After each acquisition block, the data
were stored on a personal computer. The cadence was computed from
the number of stance phases over time.
Statistical analysis. To test the significance of the differences in the
computed variables and parameters across the stepping trials of the
control block (before isometric contraction), the postcontraction 1
block, the recovery block, and the postcontraction 2 block, a two-way
repeated-measures ANOVA (blocks and trials) was used. This anal-
Fig. 4. Percent drop in maximal voluntary contraction (MVC) induced by the
tonic contraction (MVC immediately after contraction divided by MVC before
contraction period) plotted against the fatigue index for 13 subjects. Despite
great variability, the regression was significant. The best-fit line is plotted, and
its equation is reported.
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 NECK MUSCLE FATIGUE AND STEPPING IN PLACE 145

Fig. 5. A: example of body midpoint path in the working field

for one trial of one subject during the stepping in place with
eyes closed under control condition. In this case, the subject
showed a forward progression of !1 m during the 30-s stepping
trial. The step-by-step body midpoint mediolateral (M-L) os-
cillation of '10 cm is clearly evident along the x-axis. The gray
line, superimposed on the body midpoint path, is the interpo-
lated curve that minimized the squared mean error. B: projec-
tions of the instantaneous positions of the body midpoint on the
M-L (top) and anteroposterior (A-P; bottom) plane. Superim-
posed on these projections are the respective interpolated
curves.

ysis was separately performed on the two groups of subjects (fatigue
and no-fatigue groups), divided on the cluster analysis mentioned
before. To check for a significant main effect of fatigue on A-P
displacement for group, both groups were analyzed together in a
three-way ANOVA (fatigue vs. no-fatigue group, blocks and trials). A
two-way repeated-measures ANOVA (blocks and trials) was used to
test for repetition effects on A-P displacement during stepping in
place in the no-load trials; all subjects collapsed. A three-way repeat-
ed-measure ANOVA (load vs no-load, blocks and trials) in the group
of five subjects who showed the highest EMG fatigue indexes was
used for assessing possible repetition effects, as opposed to fatiguing
tonic contraction effects, on A-P displacement. When appropriate, the
Newman-Keuls test was used for post hoc comparisons. Between the
two groups, the mean indexes of fatigue and the corresponding mean
indexes of A-P displacement were compared by means of the Stu-
dents nonpaired t-test. When necessary, a linear regression analysis
was carried out. The level of significance at which the null hypothesis
was rejected was always equal to P ' 0.05.
distance covered in the forward direction was equal to 48.7 "
19.3 and 34.5 " 17.2 cm (means " SE; no-fatigue and fatigue
groups, P $ 0.56).
Qualitative effects of the isometric contraction of dorsal
neck muscles on the body midpoint path. The isometric con-
traction of the dorsal neck muscles did not produce the same
changes in the body midpoint path in all the subjects. During
the trials performed in the period after the first contraction
(postcontraction 1), some subjects basically reproduced the
same path already seen during the control blocks. It turned out
that, in these subjects, the neck muscle EMG signals during the
isometric contraction showed no or negligible signs of fatigue
and so did the index of fatigue. On the contrary, other subjects

RESULTS

Body midpoint path under control condition. The covered

path during the stepping-in-place trials was quite variable from
subject to subject, even during the block of control trials.
Nevertheless, it was possible to identify two dominant behav-
iors. Some subjects moved forward some distance along their
sagittal plane (Fig. 6, subject A). Other subjects remained
almost in place, and the movement of their body midpoint
generated a winding line covering a circumscribed area around
the starting point (Fig. 6, subject B). The behavior of each
subject was quite consistent within the trials of the control
block. The sway of the body midpoint, which was connected to
the pelvis movement during the shift of the body weight from
one foot to the other, was evident in all subjects and trials. This
was filtered out by the interpolating procedure that gave the
body midpoint path along the heading direction. Across the
subjects, large A-P displacements corresponded to long inter-
polated paths. This denotes that during the stepping-in-place
trials the predominant movement was along the A-P plane,
since, if a trial were characterized by conspicuous shifts of the
body midpoint from the straight-ahead direction, the length of
its interpolated path would be greater than the mean distance of
its A-P displacement. When all the control trials from all Fig. 6. Examples of different body midpoint displacements taken from 2
subjects, different from that of Fig. 5, during the stepping in place under
subjects were gathered into two groups, one showing and one control condition. Although subject A (A) exhibited a forward progression of
not showing EMG signs of fatigue (on the basis of the fatigue !40 cm, subject B (B) almost stepped on the spot throughout the 30-s trial. E,
index) and separately averaged, the mean value of the A-P Starting point (at y $ %140 cm and x $ 30 cm).

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146 NECK MUSCLE FATIGUE AND STEPPING IN PLACE

Fig. 7. Examples of body midpoint paths in the working field

for 2 subjects (A and B) during the stepping in place with closed
eyes under each of the 4 experimental conditions (from top to
bottom: control, postcontraction 1, recovery, and postcontrac-
tion 2). For each condition, the 2 columns correspond to the first
and last (5th) stepping trials of each subject. Under all condi-
tions, the stepping trials began at the same spot (open circle in
each graph at x $ 30 and y $ %140 cm). Subject A reversed his
forward displacement in the first trial after the first period of
isometric dorsal neck muscle contraction; in the first trial after
the second contraction period, his displacement was directed
backward. At the 5th stepping trial of postcontraction 2, the
backward displacement disappeared. Subject B moved back-
ward from the beginning, but his backward displacement was
much larger in the first trials of the postcontraction blocks 1 and
2. Also in this case, the last trials of the postcontraction blocks
were similar to the control trials.

showed a different body midpoint path from that of the control
block trials. Figure 7 shows the paths of the first and the fifth
trial of each block for two representative subjects (subjects A
and B), in whom the neck muscle EMG during the isometric
contraction showed clear-cut signs of fatigue. The graphs of
the first trial after the contraction period (postcontraction 1)
showed different paths between the first and fifth trial of the
control block. In particular, the subject who, during the control
trials, moved forward (subject A) in this first trial remained
roughly in place, just behind the starting point. During the trials
after the rest period (recovery block), the paths tended to
recuperate the feature of the control trials without really repro-
ducing it. This means that, even after a rest period of 30 min,
this subject was unable to reach a complete recovery. On the
J Appl Physiol VOL
other hand, the subject who during the control trials remained
in place (subject B) moved backward after contraction, taking
away from the starting point. The effects of the isometric
contraction were also reproduced in the first trial of the period
after the second contraction (postcontraction 2). As shown in
the bottom graphs of Fig. 7, both subjects moved backward,
farther from the starting point.
Mean A-P displacement of body midpoint in the two groups
of subjects: the effect of fatigue. The mean differences in the
A-P displacement and in the traveling direction (forward or
backward) were separately analyzed in the subjects showing
and not showing signs of fatigue based on the magnitude of the
EMG index of fatigue (see METHODS). The subjects could in fact
be clustered into two groups, which had significantly different
99 JULY 2005 www.jap.org
 NECK MUSCLE FATIGUE AND STEPPING IN PLACE
Fig. 8. For each subject, the A-P index has been plotted vs. the fatigue index
(see METHODS). An A-P index equal to zero indicates no changes in the
displacement along the A-P axis, whereas a negative value indicates a back-
ward displacement after the first isometric contraction period. Across the
subjects, the A-P indexes showed greater negative values as a function of
increasing fatigue indexes. F, Subjects of the no-fatigue group; , subjects of
the fatigue group.
J Appl Physiol VOL
147
mean indexes of fatigue (fatigue group, index of fatigue of
(1.5, 2.302 " 0.31; no-fatigue group, index of fatigue of
'1.5, 1.146 " 0.19; P ' 0.001).
The corresponding mean indexes of displacement (A-P in-
dex) were for the fatigue group %0.49 " 0.33 and for the
no-fatigue group 0.0 " 0.17 (P ' 0.05). Figure 8 shows the
A-P indexes calculated for the first stepping trial after the first
isometric contraction period vs. the fatigue index of each
subject. It is possible to appreciate that, when the fatigue index
assumed values lower than 1.5, the A-P index was very close
to zero, whereas when the fatigue index was greater than 1.5,
the A-P index assumed much lower, negative values. It can
also be seen that, despite a considerable variability, there was
a significant inverse relationship between the two indexes [the
equation of the best-fit line was y $ %0.41x & 0.46; R2 $ 0.56;
F(1,8) $ 10.473; P $ 0.011].
Figure 9 shows the mean values of the body midpoint A-P
displacements of the fatigue (Fig. 9A) and no-fatigue groups
(Fig. 9B) for each of the successive stepping trials. When both
groups were analyzed together in a three-way ANOVA (fatigue
Fig. 9. A and B: mean values (&SE) of the body
midpoint A-P displacements for all subjects of
the fatigue (A) and no-fatigue (B) group for each
of all successive stepping trials under all exper-
imental conditions. Reduction of the A-P dis-
placement is obvious in the first trials of the
postcontraction periods 1 and 2 (Post C1 and
Post C2, respectively; shaded bars) in the fatigue
but not in the no-fatigue group. C and D: mean
values (&SE) of the body midpoint M-L dis-
placements for all the subjects, grouped as
above. M-L displacements were not affected by
the contraction periods 1 and 2 in either group.
E and F: neither the first nor second contraction
period produced significant M-L deviations of
the path, as assessed by the SD (along the
x-axis) of the interpolated path. Contr, control
condition.
99 JULY 2005 www.jap.org
148 NECK MUSCLE FATIGUE AND STEPPING IN PLACE
vs. no-fatigue group, blocks and trials) to check for a signifi-
cant main effect on A-P displacement for group, no significant
differences were found between groups [F(1) $ 0.66; P $
0.44]. There was no effect for trials [F(4) $ 0.79; P $ 0.54]
and a marginal effect for blocks [F(3) $ 2.65; P $ 0.07].
However, there was an interaction between blocks and trials
[F(12) $ 2.44; P $ 0.008] and between groups, blocks, and
trials [F(12) $ 1.88; P $ 0.045]. In particular, the post hoc test
showed no difference between the trials of the control blocks of
the two groups (P ( 0.02 for all comparisons). But there were
significant differences between the two groups in the first trials
of the second blocks (postcontraction 1, P $ 0.031) and in the
first trials of the fourth blocks (postcontraction 2, P $ 0.0017).
The fatigue group was characterized by a reduced A-P
displacement in some postcontraction 1 trials as well as in
some postcontraction 2 trials with respect to the control trials.
Two-way ANOVA showed that, although there were no dif-
ferences between blocks [F(3) $ 1.999; P $ 0.168] or between
trials [F(4) $ 0.313; P $ 0.865], there was an interaction
between blocks and trials [F(12) $ 2.319; P $ 0.019]. The
post hoc test showed that the significant reduction in A-P
displacement was present for the mean values of the first trials
of the postcontraction 1 (compared with all control trials) and
2 (compared with all control and recovery trials) blocks (P '
0.03 for all comparisons). The successive trials of postcontrac-
tions 1 and 2 showed a progressive but incomplete recovery
toward control mean values.
In the subjects showing only mild or no sign of fatigue, the
A-P displacements remained unchanged across the different
blocks and trials [2-way ANOVA; blocks, F(3) $ 0.849, P $
0.493; trials, F(4) $ 0.775, P $ 0.557]. There was a significant
interaction between blocks and trials [F(12) $ 2.029; P $
0.042]: the post hoc test showed a significant effect limited to
the difference between the first trial of the last block (postcon-
traction 2 blocks) and the last trial of the control block (P $
0.030).
A-P displacement of body midpoint under no-load condition.
When the same subjects stepped in place (4 blocks of 5
subsequent stepping trials each), but this time without any
interposed period of head extensor effort (no-load session), no
effect of the repetition of the stepping trials on the body A-P
displacement was seen. The two-way ANOVA applied to the
A-P displacement of all block and trials in all subjects col-
lapsed (n $ 10) gave neither a significant main effect [blocks,
F(3) $ 2.295, P $ 0.100; trials, F(4) $ 1.116, P $ 0.364] nor
a significant interaction [F(12) $ 1.05; P $ 0.409]. The
ANOVA was then applied to the subjects belonging to the
fatigue group alone, with the aim of comparing their A-P
displacement between the two experimental conditions (iso-
metric contraction vs. no load). The three-way ANOVA (con-
dition, block, trial) gave no significant effect for conditions
[F(1) $ 0.008; P $ 0.932] and trials [F(4) $ 0.213; P $
0.930] but a main effects for blocks [F(3) $ 3.603; P $ 0.028].
There was a significant interaction (condition, block, trial)
[F(12) $ 1.983; P $ 0.034]. In particular, the post hoc test
indicated that the first trials of the second and fourth block of
the load condition exhibited a smaller A-P displacement (sec-
ond block, P $ 0.049; fourth block, P $ 0.001) than the
corresponding trials of the no-load condition.
J Appl Physiol VOL
Mean M-L displacement of body midpoint in the two groups
of subjects: the effect of fatigue. The M-L displacements,
computed as the difference between the x coordinates of the
starting and final points, were always small in the control trials
in the two groups. This behavior remained unchanged in all
subsequent trials, independently of the experimental condition
and group (Fig. 9, C and D). The two-way ANOVA applied to
the fatigue group gave neither significant main effects [blocks,
F(3) $ 0.631, P $ 0.609; trials, F(4) $ 0.573, P $ 0.686] nor
significant interaction [F(12) $ 1.903; P $ 0.058]. The two-
way ANOVA applied to the no-fatigue group gave neither
significant main effects [blocks, F(3) $ 1.603, P $ 0.240;
trials, F(4) $ 1.835, P $ 0.172] nor significant interaction
[F(12) $ 0.342; P $ 0.977]. To make sure that the subjects did
not proceed along a winding trajectory during the stepping-in-
place trials to eventually stop at a point lying along the initial
straight-ahead line, the mean standard deviation of the inter-
polated path was computed. As shown in Fig. 9, E and F,
neither contraction condition produced significant changes in
the mean standard deviation. The two-way ANOVA applied to
the mean standard deviation values of the interpolated path in
the fatigue group gave neither significant main effects [blocks,
F(3) $ 0.205, P $ 0.891; trials, F(4) $ 0.176, P $ 0.947] nor
significant interaction [F(12) $ 0.417; P $ 0.949]. The two-
way ANOVA applied to the no-fatigue group gave neither
significant main effects [blocks, F(3) $ 1.23, P $ 0.341; trials,
F(4) $ 2.146, P $ 0.122] nor significant interaction [F(12) $
1.949; P $ 0.513]. Therefore, we conclude that subjects did
not significantly deviate from a straight pathway under any
experimental condition.
Body sway during stepping in place. There were no a priori
reasons for excluding the possibility that fatigue increased the
body sway during stepping in place and that such instability, in
turn, could be at least in part be responsible for the observed
changes in the path of the postcontraction stepping trials. The
body midpoint sway around the main body midpoint direction
of displacement was evaluated on the basis of the mean
squared error made by the path interpolation. This parameter
estimated how much the actual path differed from the interpo-
lated path and, therefore, to what extent the subjects swayed on
the spot by moving the body weight from one foot to the other
during stepping in place. As shown in Fig. 10, A and B, fatigue
did not increase body sway, neither in the A-P axis nor on the
M-L axis. The two-way ANOVA applied to the A-P data of the
fatigue group gave neither significant main effects [blocks,
F(3) $ 0.404, P $ 0.753; trials, F(4) $ 0.786, P $ 0.551] nor
significant interaction [F(12) $ 0.779; P $ 0.668]. The two-
way ANOVA applied to the M-L data of the fatigue group gave
neither significant main effects [blocks, F(3) $ 2.013, P $
0.166; trials, F(4) $ 1.013, P $ 0.430] nor significant inter-
action [F(12) $ 1.907; P $ 0.057].
Head position during stepping in place. The position of the
head was measured to check whether the isometric contraction
of the dorsal neck muscles provoked flexion or extension of the
head, since these modifications could be one of the possible
causes of the fatigue-induced variations of the path. The mean
values of pitch angle as well as roll angle did not show
differences among the trials (Fig. 11). The two-way ANOVA
applied to the pitch angle data of the fatigue group gave neither
significant main effects [blocks, F(3) $ 1.715, P $ 0.217;
trials, F(4) $ 1.68, P $ 0.951] nor significant interaction
99 JULY 2005 www.jap.org
 NECK MUSCLE FATIGUE AND STEPPING IN PLACE
Fig. 10. Body midpoint sway around the main body midpoint direction of
displacement was obtained by the interpolation of the actual path and the
computation of its mean squared error (MSE). The average value (&SE) of
MSE is shown for all trials of the subjects belonging to the fatigue group.
Fatigue (either Post C1 or Post C2 trials; shaded bars) did not increase body
sway either in the A-P (A) or M-L axis (B).
J Appl Physiol VOL
149
[F(12) $ 1.041; P $ 0.428]. The two-way ANOVA applied to
the pitch angle data of the no-fatigue group gave neither
significant main effects [blocks, F(3) $ 1.749, P $ 0.210;
trials, F(4) $ 0.647, P $ 0.637] nor significant interaction
[F(12) $ 1.037; P $ 0.432]. The two-way ANOVA applied to
the roll angle data of the fatigue group gave neither significant
main effects [blocks, F(3) $ 1.780, P $ 0.204; trials, F(4) $
0.309, P $ 0.867] nor significant interaction [F(12) $ 0.547;
P $ 0.872]. The two-way ANOVA applied to the roll angle
data of the no-fatigue group gave neither significant main
effects [blocks, F(3) $ 0.508, P $ 0.684; trials, F(4) $ 0.201,
P $ 0.934] nor significant interaction [F(12) $ 1.952; P $
0.051]. Therefore, the isometric contraction of the dorsal neck
muscles, even when it reached a fatiguing level, did not affect
the position of the head during stepping in place.
Stepping-in-place cadence. The mean stepping cadence un-
der control conditions was not significantly different between
the fatigue and the no-fatigue groups (54.0 " 3.5 and 59.3 "
5.2 steps/min, respectively). There were minor effects of iso-
metric neck muscle contraction on stepping cadence. The
two-way ANOVA applied to the fatigue group gave neither
significant main effects [blocks, F(3) $ 2.172, P $ 0.144;
trials, F(4) $ 0.185, P $ 0.943] nor significant interaction
[F(12) $ 1.645; P $ 0.111]. The two-way ANOVA applied to
the no-fatigue group gave a significant main effects for trials
[blocks, F(3) $ 0.217, P $ 0.883; trials, F(4) $ 3.347, P $
0.036] but no significant interaction [F(12) $ 0.849; P $
0.602]. The significant changes between trials in cadence in the
no-fatigue group were due to a very minor augmentation from
the first to the last trials (from 59.7 to 60.3 steps/min, all blocks
collapsed), i.e., to less than one additional step over the entire
period (30 s) of acquisition. To further check that even any
nonsignificant variation in cadence in the fatigue group could
be one of the possible causes of the path alteration and of the
A-P displacement reduction during the first trial of postcon-
Fig. 11. Mean values (&SE) of the head
pitch angle (A and B) and head roll angle (C
and D) for all the subjects of the fatigue (A
and C) and no-fatigue (B and D) groups for
each of all successive stepping trials under all
experimental conditions. The mean angles
were not different among the trials of either
group.
99 JULY 2005 www.jap.org
150 NECK MUSCLE FATIGUE AND STEPPING IN PLACE
traction 1 and postcontraction 2, the A-P index was plotted vs.
the percent cadence change in the first trial after fatigue (with
respect to the mean cadence in the 5 control trials) for each
subject of the fatigue group. The regression analysis gave no
significant relationship [R2 $ 0.0002; F(1,3) $ 0.00067; P $
0.981].
DISCUSSION
During stepping in place, before the prolonged head exten-
sor effort, the subjects presented a substantial variability in
their behavior. Most of them had a tendency to slowly proceed
along the subjects sagittal plane, and some showed a mild
M-L displacement. Only a few subjects really did step in place.
Across the subjects, the mean progression of the body midpoint
was in the forward direction, whereas the displacement in the
M-L direction was, on average, close to zero. In all cases, no
subject was aware of his or her displacement in the walking
space. The extent of the forward progression of the subjects
changed significantly after the 5-min period of tonic contrac-
tion of the dorsal neck muscles. In turn, the extent of this
change depended on the degree to which the contraction
produced muscle fatigue in the neck muscles.
Because the EMG can furnish an indirect measure of fatigue
in the muscle of interest under conditions of controlled isomet-
ric contraction (64), an EMG index was used to quantify the
muscle contraction level across the subjects. This index de-
pended on EMG changes in both amplitude and median fre-
quency occurring during the period of isometric dorsal neck
muscle contraction. Indeed, the changes in these two variables
were highly correlated within several subjects of our popula-
tion, regardless of gender and weight, whereby the EMG
amplitude gradually increased together with a gradual decrease
in EMG median frequency during the contraction period. In
other subjects, this correlation was not evident, since EMG
amplitude and median frequency showed no sizeable changes
during the contraction period. The relationship between EMG
index and fatigue was also shown by the significant regression,
across 13 subjects, between the percent decrease in MVC
produced by the tonic contraction and the fatigue index. On
these bases, we assumed that the EMG index was a good
marker of muscle fatigue, and we used it for dividing all our
subjects into two subgroups.
In the subjects showing EMG signs of neck muscle fatigue,
the forward displacement during the stepping-in-place trials
proved to be much reduced (to 32%, on average) immediately
after the 5-min period of tonic contraction with respect to the
stepping trials performed under control conditions. Some sub-
jects even stepped in the backward direction. This behavior
was obvious only in the first trial immediately after the fatigu-
ing period, a sign of relatively rapid recovery from the fatigue
effects, in keeping with recent reports from other investigations
(16). However, it was reproduced and even enhanced in the
first trial of the second series of the stepping trials performed
after the second fatiguing session, where the average displace-
ment was in the backward direction. This would point to a
residual effect of the first fatiguing contraction that had not
completely vanished at the end of the recovery period of 30
min and added to the effects of the second fatiguing contraction
(67). Shorter bouts of back muscle fatiguing contraction re-
cover earlier (41). This behavior was not obvious in those
J Appl Physiol VOL
subjects for whom dorsal neck muscle contraction did not show
or showed only minor EMG signs of fatigue.
All subjects also participated in an additional session, when
they were asked to step in place and perform the same se-
quence of blocks and trials but without the tonic isometric
contraction of the dorsal neck muscles (no-load session). The
repetition of the stepping trials per se did not produce signif-
icant effects on the body displacement. This strengthens the
notion that the cause of the observed reduced forward progres-
sion or backward displacement was the neck muscle contrac-
tion rather than some process connected with the repetition of
the trials or with the feedback received by subjects being
repositioned at the starting point after each trial.
When we searched for a graded change in the body progres-
sion along the sagittal plane by plotting the A-P index of
displacement against the EMG index of fatigue, it turned out
that, despite a considerable variability (likely connected to
individual anthropometric characteristics, to peculiarity of the
stepping task, and to the magnifying effects of the ratios used
for computing the indexes), the relevant changes in the dis-
placements along the sagittal plane after contraction were again
evident only in the subjects in whom the contraction produced
clear-cut EMG signs of fatigue. This finding is also in favor of
a rather selective role of fatigue, rather than prolonged con-
traction per se, in producing the effects and also strengthens the
EMG criteria for separating the subjects into two groups.
Body unsteadiness during stepping? Dorsal neck muscle
contraction, be it fatiguing or not, did not produce abnormal
oscillations around the interpolated stepping path of the body
midpoint during stepping, which would happen if a subjects
body midpoint became unusually unsteady around the mean
position. This might have been assumed on the basis of a
previous study, in which dorsal neck muscle fatigue was able
to produce moderate but significant increases in body sway
during quiet stance (4). It should be noted, however, that the
increase in body sway during quiet stance that was described in
that paper was not associated with any major change in the
center of foot pressure (forward, backward, or sideways),
which might have entrained directional effect in the body
displacement during the stepping in place. However, any cor-
respondence between body oscillations under static (quiet bi-
pedal stance) and dynamic condition (stepping in place) must
be considered with caution, because in the latter case balance
control heavily depends on the alternate shift of the body
weight on a single support.
The fatigue-induced changes in the A-P displacement during
the stepping-in-place task were not dependent on changes in
head posture. In fact, head position did not change postcon-
traction, either in pitch or roll angle, either with or without
signs of fatigue. The fact that the head remained in place
despite the fatigue of the head extensor muscles was likely
dependent on the very low level of force necessary to coun-
teract the gravity-dependent head flexion, a level of force
easily produced even by heavily fatigued muscles. Possibly,
the production of the appropriate dorsal neck muscle tone was
also aided by a mechanism of minimization of the change in
the discharge from the gravito-inertial labyrinthine receptors.
Certainly, vision could not help, since the subjects were blind-
folded during the stepping phase. In turn, the absence of
excessive body midpoint oscillations during stepping could be
favored by a mechanism of head-referenced body stabilization,
99 JULY 2005 www.jap.org
 NECK MUSCLE FATIGUE AND STEPPING IN PLACE
the importance of which in the postural control system and
inertial guidance of locomotion has been already emphasized
by Pozzo and coworkers (53).
Putative neural mechanisms. Neck muscles are surely cen-
tral in the construction of a reference frame for movement in
space. Such a role is apparently not played by the leg muscles
involved in the production of body movement, at least as
indicated by the minor effect of bilateral triceps surae vibration
during walking (13). It is therefore in that light that we would
like to propose an explanation of the observed phenomenon. In
so doing, it seems useful to discuss the present data, together
with those of the studies describing the effects of dorsal neck
muscle vibration, in the line of the process of multisensory
fusion that leads to egocentric space representation.
During stepping in place, neck vibration produces involun-
tary forward stepping at about 0.3 m/s without modifying the
stepping frequency (32). In our case, neck muscle fatigue
instead induced an involuntary smaller forward progression or
even backward progression. The difference between the effects
of fatigue and vibration cannot be ascribed to the more aspe-
cific distribution of fatigue, since the concurrent EMG record-
ing from the anterior neck muscles showed no sign of activa-
tion of these muscles. Similar to vibration, the stepping ca-
dence did not undergo major changes as a consequence of neck
muscle fatigue. The small changes in cadence observed were
unrelated to the distance or direction of body displacement
during the stepping. Apparently, the central effects of both
vibration and fatigue do not influence the rhythmic outflow
from the central pattern generators implicated in this automatic
locomotor-like stepping activity.
Perhaps, the changes in body progression along the sagittal
plane should be attributed to the outflow from the neck muscles
to the brain centers responsible for building the body spatial
reference frame. Vibration and fatigue both produce modifica-
tions in joint position sense (for vibration, see Refs. 9, 20, 22,
30, 31; for fatigue, see Refs. 12, 16, 24, 26, 57, 59). This
testifies of the capacity of the afferent input from dorsal neck
muscles of accessing the central nervous system and altering
the perception of the position of the segments in space. How-
ever, the fatigue state and vibration effects dramatically di-
verge as far as the modification in the presumed reference
frame for controlling locomotion is concerned. Fatigue reduces
the forward distance reached by subjects who normally exhibit
a forward progression and pushes clearly backward those who
stepped in place.
This would speak in favor of a different set of receptors and
afferent fibers under vibration and fatiguing contraction con-
ditions, indirectly or directly responsible for the modulation of
the reference frame. In particular, the receptors responsible for
the shrinkage of our imagined space in the forward direction
or for the backward displacement of the body position
reference after fatigue would be different from those possibly
activated by muscle contraction per se (like tendon organs or
muscle spindles). Rat experiments have shown that fatigue
activates small-fiber receptors, the same that are activated by
capsicine (52). Small-fiber sensory input may be the result of
an increased inflow from the free nerve endings as a conse-
quence of ionic or metabolic changes (elevated interstitial
potassium concentration or insufficient oxygen availability due
to reduced blood flow) (19, 52). This input, in addition to
inhibiting muscle spindle afferent activity during fatigue (10),
J Appl Physiol VOL
151
could also directly access the brain centers responsible for
shaping our reference frames for navigation. Interestingly,
abnormal conditions of the neck muscle (tension neck) can
disrupt the normal postural response to neck muscle vibration
(40), pointing to a susceptibility of the reference system to
abnormal fatigue-related inputs of neck muscle origin.
Admittedly, fatigue can affect the discharge of many sensory
receptors, including muscle spindles (27, 34, 63, 64, 67). In
turn, spindle discharge could be modulated by fatigue-induced
alterations in gamma-motoneuron discharge (43, 51). Such
abnormal muscle spindle inflow could possibly perturb and
deteriorate postural control through an action on the central
nervous system (19). However, one may note that there was no
neck muscle contraction during the stepping trials and presum-
ably little spindle discharge, since the latter should not outlast
previous contraction, contrary to the discharge of the receptors
sensitive to fatigue-induced intramuscular changes. Any mod-
ulation of a scarce proprioceptive input would therefore hardly
produce the gross effects shown here in body progression,
emphasizing a direct effect of fatigue-related input as a cause
of the abnormal progression after the fatiguing contraction.
Neck muscle fatigue effects on locomotion. Stepping in place
with closed eyes and without acoustic cues is a nonoptimal
definition for a locomotor task and presents itself with peculiar
characteristics from subject to subject (7). The drift from the
starting position is a sign of unreliable feedback during step-
ping in place (61). Most likely, many sensory modalities
normally able to convey velocity and direction information,
such as the foot sole receptors and their central integration, are
below the threshold under these circumstances, or the central
mechanisms for calculating the mismatch between the succes-
sive positions of the two leg can be fooled by the minimal
differences of their positions between steps. The gravito-
inertial receptors would also be of no use, given that the
successive head and body up and down movements do not
seem to be influenced by the body progression and that the
linear body velocity in the midsagittal plane is negligible even
when it reaches its maximum value (!3 cm/s) (25). Certainly,
no subject was aware of his or her displacement in the working
space, either before or after the fatigue-induced effects. And
this comes as no surprise, since much larger body displacement
produced by lateral neck muscle vibration during stepping in
place went completely unnoticed by the subjects (4). There-
fore, the body displacement would be the expression of the
spontaneous drift in the activity of the brain centers controlling
the body position in space. This command center, although
numb to the afferent sensory input from the evolving move-
ment, is, however, sensible to other afferent inputs like that
from fatigued neck muscles. Despite the highly variable body
displacement across subjects, the relative consistency of this
displacement in the different trials within a subject could be
taken as an indication that the subjects reference for the
stepping position can be relatively stable. It seems, therefore,
that stepping in place after neck muscle fatigue is being
performed with respect to a reference system and modified in
the same sense by the fatigue-induced input in every subject.
Such a modification could be reminiscent of an error of
parallax, as if the brain would incorporate depth information
when it updates its stored representations of space after the
neck muscle fatiguing contraction (45).
99 JULY 2005 www.jap.org
152 NECK MUSCLE FATIGUE AND STEPPING IN PLACE
ACKNOWLEDGMENTS
The help of M. V. Beretta and A. M. De Nunzio during data collection is
gratefully acknowledged. We thank two unknown referees for critical reading
and detailed suggestions.
GRANTS
This work was supported by grants from the Italian Ministry of Health
(Ricerca Finalizzata 2002) and Ministry of University and Research (Progetto
Ricerca Interesse Nazionale 2003, Fondo Investimenti Ricerca di Base 2002).
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