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Eur J Appl Physiol (2009) 107:73–81
DOI 10.1007/s00421-009-1097-3
123
ORIGINAL ARTICLE
Cervical proprioception is suYcient for head orientation
after bilateral vestibular loss
Eva-Maj Malmström · Mikael Karlberg ·
Per-Anders Fransson · Johannes Lindbladh ·
Måns Magnusson
Accepted: 18 May 2009 / Published online: 9 June 2009
© Springer-Verlag 2009
Abstract The aim was to investigate the relative impor-
tance of cervical proprioception compared to vestibular
input for head movements on trunk. Subjects with bilateral
vestibulopathy (n= 11) were compared to healthy controls
(n= 15). We studied their ability to move the head accu-
rately to reproduce four speciWed target positions in the
horizontal yaw plane (neutral head position, 10° target, 30°
target, and 30° target with oscillating movements applied
during target introduction). Repositioning ability was cal-
culated as accuracy (constant error, the mean of signed
diVerences between introduced and reproduced target) and
precision (variable error, the standard deviation of diVer-
ences between introduced and reproduced targets). Subjects
with bilateral vestibulopathy did not diVer signiWcantly
from controls in their ability to reproduce diVerent target
positions. When the 30° target position was introduced with
oscillating movements, overshoot diminished and accuracy
improved in both groups, although only statistically signiW-
cantly when performed towards the right side. The results
suggest that at least in some conditions, accurate head on
trunk orientation can be achieved without vestibular
information and that cervical somato-sensory input is either
up-regulated as a compensatory mechanism after bilateral
vestibular loss or is important for such tasks.
Keywords Vestibular diseases · Cervical spine ·
Cervical proprioception · Vertigo · Musculoskeletal system ·
Orientation
Introduction
Cervical proprioceptive and vestibular sensory input,
together with vision and hearing, provide necessary infor-
mation for perception of head movements and head orienta-
tion in space (Angelaki and Cullen 2008; Lackner and
DiZio 2005). Sensorimotor integration makes it possible to
interpret body orientation in space and to maintain postural
control during movement (Mergner et al. 2001; Peterka and
Loughlin 2004; Wolpert et al. 1995).
Malfunction in one sensory system may be compensated
for by the other sensory systems (Buchanan and Horak
2001; Curthoys 2000; Lacour et al. 1997; Schweigart et al.
2002; Yagi et al. 2000) and by the brain weighting sensory
information diVerently (Curthoys and Halmagyi 1995;
Lacour et al. 1997; Peterka and Loughlin 2004), but com-
plete restitution of sensorimotor function by these means is
less common (Allum et al. 2008; Buchanan and Horak
2001; Curthoys 2000; Karlberg and Magnusson 1998;
Zingler et al. 2008). A vestibular debility increases depen-
dence on the remaining sensory inputs. Generally, compen-
sational mechanisms increase the importance of visual
(Lacour et al. 1997) and cervical proprioceptive (Yagi et al.
2000) inputs. The high concentration of proprioceptors in
the muscles (Richmond et al. 1999) and the zygapophyseal
joints of the upper neck (Richmond and Bakker 1982;
Wyke 1979) and the close interaction between the neck and
the vestibular (Mergner et al. 1997) and visual systems
(Mergner et al. 2001), underpin the theoretical assumption
that cervical sensory information is important for spatial
orientation.
To gain insight into the capacity and relative contribu-
tion of the diVerent sensory inputs, it is useful to investigate
sensorimotor function where there is a temporary or perma-
nent loss of any one of the sensory systems. This can be
E.-M. Malmström (&) · M. Karlberg · P.-A. Fransson ·
J. Lindbladh · M. Magnusson
Clinical Sciences, Lund University, Lund, Sweden
e-mail: eva-maj.malmstrom@med.lu.se
74 Eur J Appl Physiol (2009) 107:73–81
123
achieved either by excluding information from subjects
(e.g. using blindfolds or earplugs) or by doing tests in sub-
jects disabled in one or another of the sensory functions.
While complete proprioceptive loss is extremely uncom-
mon, there are subjects with loss of vestibular function. A
bilateral vestibulopathy (BV) is a rare condition with bilat-
eral loss of vestibular function (Zingler et al. 2007). Key
symptoms for BV are unsteadiness, especially of gait, and
blurred vision caused by oscillopsia during head move-
ments (Brandt 1996).
The importance of proprioceptive input for compensa-
tion after vestibular lesions has been assessed by evaluating
sway parameters (Allum et al. 2008; Lacour et al. 1997),
body orientation (Earhart et al. 2004; Weber et al. 2002)
and postural control (Buchanan and Horak 2001).
Presently, there are no objective tests to assess cervical
proprioception. However, psychometric head repositioning
tests make indirect evaluations possible (Loudon et al.
1997; Revel et al. 1991). Head repositioning tests have
been used to evaluate neck disorders (Lee et al. 2008;
Loudon et al. 1997; Revel et al. 1991) and neck treatment
interventions (Heikkila et al. 2000; Palmgren et al. 2006;
Revel et al. 1994) and to increase the understanding of pro-
prioception under diVerent experimentally induced sensory
conditions (Owens et al. 2006). The rationale for head repo-
sitioning tests is that head movements on trunk are sensed
by proprioception (Loudon et al. 1997; Revel et al. 1991).
However, head movements will always stimulate the ves-
tibular sensors as well (Fransson et al. 2000). One recent
study with repositioning to neutral head position (NHP)
found no diVerences between a BV group and healthy con-
trols (Pinsault et al. 2008b), while a study of patients with
unilateral vestibular loss did (Treleaven et al. 2008).
With conXicting results of repositioning tests for subjects with
vestibular lesions, the importance of and relation between ves-
tibular and cervical sensory input still remain unclear.
The aim of this study was to investigate whether subjects
with bilateral vestibulopathy maintain their ability to recog-
nize and Wne-tune head movements on a stable trunk or if
their perception of head on trunk movements is impaired.
Methods
Subjects
We studied 11 subjects with bilateral vestibulopathy (BV)
(8 men, 3 women, mean age 51 years, range 24–74), previ-
ously diagnosed at the Department of Otorhinolaryngology
of Lund University Hospital, Lund, Sweden. The bilateral
vestibulopathy was established with head impulse tests
(Halmagyi and Curthoys 1988), bithermal and ice water
caloric tests, and vestibular evoked myogenic potentials
(Colebatch et al. 1994). Causes for vestibulopathy were
autoimmune disease (n= 3), neurosarcoidosis (n=1),
sequential vestibular neuritis (n= 1), ototoxic medication
(n= 1), and idiopathy (n= 5). Time since diagnosis varied
between 6 months and 9 years (mean 5 years). The BV
patients were compared to a control group (8 men, 7
women, mean age 45 years, range 29–74), with no vestibu-
lar or cervical problems. All subjects in the control group
identiWed themselves as ‘neck healthy’. The control group
was recruited through advertisements or through personal
invitation at their place of work or site of recreational activ-
ity. In the BV group, two reported some previous cervical
problems (neck pain and reduced cervical range of motion
[CROM]), which had required previous physical treatment.
In each subject, the musculoskeletal neck was examined
to exclude major dysfunctions or pain. The examination
consisted of lateral Xexion of the head to test mobility of
upper segments, manual palpation of the spinal process of
C7 during active head rotation to test mobility of the cerv-
ico-thoracic junction, and palpation of any tenderness in the
sternocleiodomastoid, trapezius, levator scapula, and sub-
occipital muscles. No major tenderness or decreased mobil-
ity was found in any of the subjects. CROM values for the
BV group did not diVer from those of the controls (right
rotation: BV group: 67.1 §7.6°, controls: 69.1 §8.6°; left
rotation: BV group: 63.1 §7.7°, controls 67.2 §8.3°),
which further conWrms comparable cervical conditions
between the groups.
All subjects gave their written informed consent to par-
ticipate in the study and were informed that they could stop
the test at any time, for any reason. They were compensated
with approximately 42 euros for participating. The study
design was approved by the Regional Ethics Review Board
in Lund (411/2006), Lund University, Lund, Sweden.
Head repositioning test device
Head movements relative to the trunk were recorded with
Zebris®, a three-dimensional ultrasound device (Zebris®-
CMSHS, and software WinSpine, version 1.78; Zebris
Medizintechnik GmbH, Isny, Germany) (Dvir and Prushansky
2000; Lee et al. 2006; Malmstrom et al. 2003). The Zebris®
head device, a helmet, was fastened on the subject’s head
with a Velcro closing, and the reference shoulder cap was
attached to the right shoulder. A bathing cap was placed
underneath the Zebris® helmet to minimize directional
information from the tester’s hands during target position
introduction. The ultrasound microphones on the helmet
and shoulder cap received signals from three transmitters
on a frame positioned approximately 1 m to the right of the
subject. The sampling frequency was 50 Hz. The Zebris®
measures the distances to the microphones by timing of the
interval between the emission and the reception of
Eur J Appl Physiol (2009) 107:73–81 75
123
ultrasound pulses. The absolute 3D coordinates are then
calculated by triangulation.
Procedure
Before the test, subjects received uniform instructions from
a video describing the protocol. Subjects were seated on a
stool with a 10° slope and asked to assume a posture in
which the centre of mass was projected through a plane
intersecting both tuber ischii. Slumped posture was cor-
rected and the subjects’ hands were placed on their thighs.
Subjects were asked to keep this position throughout the
test.
To check the attachment of the devices and as a warm
up, the subjects performed four maximal head rotations,
starting toward the right. Thereafter, CROM in horizontal
yaw rotation was recorded four times with Zebris®
(Malmstrom et al. 2003, 2006). The mean of these four
measurements was then used as the CROM for the individ-
ual in further analysis.
The movements used in the tests were about half of the
CROM. The introduced 30° target to the right side was on
average 46% §6 (mean §SD) of the CROM in the BV
group and 45% §7 in the control group. To the left side, it
was on average 49% §6 in the BV group and 46% §5 in
the control group.
Following this pretest, the subjects were blindfolded and
had ear plugs inserted to minimize external information
cues. The repositioning targets were 10° (10°TAR), 30°
(30°TAR) (Loudon et al. 1997), 30° with oscillating hori-
zontal head movements of approximately 2 Hz and 10°
amplitude applied by the tester when introducing the target
position (30°TAR-osc) (Fig. 1), and NHP (Revel et al.
1991), all in the horizontal yaw plane. Targets were ran-
domly introduced by the drawing of lots before the test
occasion. Tests were randomized by lots to start towards
right or left side equally frequently (26 subjects; 13 right/13
left as starting side). Target positions were introduced by
the tester moving the head of the subject to the target posi-
tion. This was guided by Zebris® real-time onscreen record-
ing. The position was held for more than 3 s and explicitly
designated as the goal; subjects were requested to memo-
rize the introduced target position. The head was moved
back to starting position by the tester and the subjects per-
formed repositioning to the target three times. Subjects per-
formed the repositioning tasks at their own pace. NHP was
recorded after active head movement from starting position
(refNHP) to maximum rotation and the return to perceived
NHP (Revel et al. 1991). Starting position (refNHP) was
deWned when the subject kept the head in the sagittal and
frontal plane according to the subject’s judgement of
‘straight ahead’ before testing. Before each position test,
the starting position was calibrated to zero in the Zebris®
system.
Subjects signalled verbally when they considered
themselves to be at TAR/NHP and each repositioning was
deWned in the recording by the tester interrupting the
ultrasound waves with a wave of the hand. This caused
spikes in the recording, which were used to identify the
reproduced positions (Fig. 2). IdentiWcation of the goal
position was made from the plateau in the recordings when
the head was held still during the introduction. RefTARs
and refNHPs were deWned from mean values from 1 second
of registration of this plateau (Fig. 2).
Fig. 1 Introduction of 30° target with and without oscillating head
movements applied. The oscillating movements were performed by the
tester both in the direction towards and from the introduced target with
a frequency of about 2 Hz
Fig. 2 Procedure of 30° target
identiWcation. Introduction of
target with 1 s selected (A) from
which the mean value was deW-
ned as refTAR. IdentiWcation of
reproduced targets (individual
lines) was made immediately
before the spikes (B). Spikes
were caused by tester interrupt-
ing ultrasound waves with hand
movements when subjects
verbally signalled they
considered themselves to be at
target
76 Eur J Appl Physiol (2009) 107:73–81
123
Reliability of the position identiWcation procedure was
tested between two testers who identiWed targets indepen-
dently (in Wve BV and ten controls). In all, 90 target variables
(15 subjects £3 reproduced trials £2 sides) for each target
were compared. The identiWcation procedure was consistent
for the two testers, with average intraclass correlation coeY-
cient (ICC) values of 0.985–0.998 and mean diVerences of
0.04–0.57°. It should be pointed out that the values used in the
study emanate from the analysis of one tester only (EMM).
The test sequence took about 45 min per subject.
Data processing and statistical analyses
The diVerences between the reproduced positions were cal-
culated in relation to the introduced goal position. When
the reproduced TAR/NHPs surpassed the introduced ref-
TAR and refNHP, they were considered overshoots and
assigned positive values. When the reproduced TAR/NHPs
were underestimated relative to refTAR/refNHP, they were
considered as undershoots and assigned negative values.
To analyze accuracy and directional bias of the reposi-
tioning tests, constant error (CE) was analyzed. Constant
error was the mean of three signed diVerences: ([TAR1 ¡
refTAR] + [TAR2 ¡refTAR] + [TAR3 ¡refTAR])/3 and
([NHP1 ¡refNHP] + [NHP 2 ¡refNHP] + [NHP 3 ¡ ref-
NHP])/3, retaining CE for TAR (CETAR) and for NHP
(CENHP) for each subject.
To analyze the variability within the performance,
expressed as the precision of the repositioning tests, variable
error (VE) was analyzed. Variable error was the standard
deviation (SD) of three signed diVerences, retaining VE for
TAR (VETAR) and for NHP (VENHP) for each subject.
A combined assessment of accuracy and precision, a
measure of overall accuracy, was deWned as the absolute
error (AE) and calculated as the mean of three unsigned
diVerences, retaining AE for TAR (AETAR) and for NHP
(AENHP) for each subject.
Parametric tests were chosen after normal distributions
were assured by Kolmogorov–Smirnov tests and inspection
of histograms. Since the BV group was not evenly distrib-
uted by gender and since there were minor age diVerences
between the groups, analyses were made both with and
without adjustments for gender and age, i.e. using gender
and age as covariates.
For intergroup comparisons the independent t test was
used. Equal variances were assumed (checked with
Levene’s test) in report of p values.
A level of p< 0.05 was chosen for statistical signiWcance
and two-tailed p values are reported. All statistical tests were
performed using SPSS 14.0 software (SPSS Inc., Chicago, IL,
USA).
Results
Accuracy, expressed as CE for directional bias, did not
diVer signiWcantly between the groups at the 10° and 30°
target positions (Table 1). Constant error (CE) for the NHP,
Table 1 Constant error for 10° target (TAR), 30° target, 30° target with oscillating (osc) movements during introduction and neutral head position
(NHP)
Subjects with bilateral vestibulopathy (BV) are compared to controls. Values are reported in degrees. Mean (Mn), standard deviation (SD), stan-
dard error of the mean (SEM), 95% conWdence interval (CI) and p values are shown
Equal variances assumed (Levene’s test > 0.05) in t test. Uncorrected and corrected p values (adjusting for age and gender eVect; age and gende
r
as covariates) are reported
BV (n= 11) Controls (n= 15) Independent t test
Controls-BV Uncorrected Corrected
Mn (SD) SEM Mn (SD) SEM 95% CI p value p value
10° TAR
Right 8.0 (3.4) 1.0 5.3 (4.0) 1.0 ¡5.7–0.4 0.084 0.219
Left 5.5 (7.1) 2.1 3.7 (3.5) 0.9 ¡6.2–2.5 0.394 0.450
30° TAR
Right 6.2 (4.3) 1.3 6.3 (5.8) 1.5 ¡4.2–4.4 0.962 0.583
Left 4.8 (3.4) 1.0 5.2 (5.5) 1.4 ¡3.5–4.3 0.825 0.715
30° TAR
Right osc 0.2 (8.7) 2.6 2.1 (6.8) 1.8 ¡4.4–8.2 0.542 0.519
Left osc 1.0 (8.2) 2.5 2.0 (6.0) 1.6 ¡4.7–6.8 0.719 0.892
NHP
Right ¡1.6 (3.3) 1.0 1.1 (4.0) 1.0 ¡0.4–5.7 0.090 0.021
Left 0.4 (3.2) 1.0 1.9 (3.0) 0.8 ¡0.9–4.1 0.209 0.173
Eur J Appl Physiol (2009) 107:73–81 77
123
when subjects rotated from maximal right yaw position to
centre, was signiWcantly diVerent between the groups after
adjustments for age and gender, but this signiWcance was
not found for uncorrected values. In post hoc analyses, it
was found that this signiWcant diVerence originated from
values with more undershoots for NHP in the BV group
(Table 1).
Constant error (CE) when oscillating head movements
were applied during introduction of the 30° rightward target
was signiWcantly decreased in comparison to target intro-
duction without oscillation for both groups (BV p=0.044;
controls p= 0.031) (Table 2).
Analyses of VE did not diVer signiWcantly between the
BV and control group (Tables 3, 4).
Overall accuracy, expressed as AE, did not diVer signiW-
cantly between the BV and control group (Tables 5, 6).
Discussion
Subjects with bilateral vestibulopathy do not diVer signiW-
cantly from controls when they move their head on trunk at
their own speed to a speciWed target position in the horizon-
tal yaw plane. The BV group tended to undershoot back to
NHP for one side (right to centre), but in all other positions,
an overshoot was seen on average.
Our results suggest that cervical proprioception is of
greater importance than vestibular information to head on
trunk orientation in the horizontal yaw plane, in accordance
with recent Wndings (Pinsault et al. 2008b). Cervical propri-
oception is vital for head movement perception and
becomes slightly more accurate when cervical and vestibu-
lar inputs are combined (Nakamura and Bronstein 1995).
Table 2 Constant error for 30° target, target introduction with no
oscillating head movements compared with oscillation
Subjects with bilateral vestibulopathy (BV) and controls are reported
separately. Mean diVerence with 95% conWdence interval (CI) and
p
values are shown
BV group Controls
Mean diV
(95% CI), p value
Mean diV
(95% CI), p value
30° target right (°) 6.0 (0.2–11.7), 0.044 4.2 (0.5–7.9), 0.031
30° target left (°) 3.8 (¡1.8–9.4), 0.158 3.2 (¡1.8–8.2), 0.187
Table 3 Variable error for 10° target (TAR), 30° target, 30° target with oscillating (osc) movements during introduction and neutral head position
(NHP)
Subjects with bilateral vestibulopathy (BV) are compared with controls. Values are reported in degrees. Mean (Mn), standard deviation (SD), stan-
dard error of the mean (SEM), 95% conWdence interval (CI) and p values are shown
Equal variances assumed (Levene’s test > 0.05) in t test. Uncorrected and corrected p values (adjusting for age and gender eVect; age and gende
r
as covariates) are reported
BV (n= 11) Controls (n= 15) Independent t test
Controls-BV Uncorrected Corrected
Mn (SD) SEM Mn (SD) SEM 95% CI p value p value
10 TAR
Right 2.6 (0.9) 0.3 1.9 (1.1) 0.3 ¡1.5–0.2 0.117 0.194
Left 2.3 (1.5) 0.5 1.7 (1.4) 0.4 ¡1.8–0.6 0.294 0.370
30 TAR
Right 3.1 (1.5) 0.5 2.3 (1.3) 0.3 ¡2.0–0.3 0.157 0.112
Left 2.6 (1.0) 0.3 2.3 (0.8) 0.2 ¡1.1–0.4 0.311 0.305
30 TAR
Right osc 2.2 (1.6) 0.5 2.6 (2.5) 0.6 ¡1.4–2.1 0.671 0.531
Left osc 2.8 (1.7) 0.5 2.7 (1.7) 0.4 ¡1.5–1.2 0.774 0.756
NHP
Right 2.2 (0.5) 0.1 2.0 (1.2) 0.3 ¡1.0–0.6 0.621 0.793
Left 1.8 (1.6) 0.5 1.4 (1.1) 0.3 ¡1.5–0.6 0.421 0.243
Table 4 Variable error for 30° target, target introduction with no
oscillating head movements compared with oscillation
Subjects with bilateral vestibulopathy (BV) and controls are reported
separately. Mean diVerence with 95% conWdence interval (CI) and
p
values are shown
BV group Controls
Mean diV
(95% CI), p value
Mean diV
(95% CI), p value
30° target right (°) 0.9 (¡0.4–2.1), 0.161 ¡0.3 (¡2.1–1.5), 0.714
30° target left (°) ¡0.2 (¡1.4–0.9), 0.685 ¡0.4 (¡1.3–0.6), 0.389
78 Eur J Appl Physiol (2009) 107:73–81
123
When subjects with BV move, they need to use information
from sensory inputs that can supplement for shortcomings
of the vestibular system. Our results suggest that cervical
proprioception contributes with signiWcant information for
head orientation during slow head movements in subjects
with vestibular loss.
The ability to identify the 30° target position after oscil-
lating movements during introduction was more accurate
(lower CE) in both groups, compared with introduction
without oscillation. Therefore, despite the ‘noise’ of oscil-
lation in target introduction, proprioceptive information
seemed to be suYcient or even enhanced by this additional
input. The purpose of moving the head to the goal position
with oscillating movements was to confuse the subjects and
reduce their ability to calculate the position from the trajec-
tory with either or both vestibular and proprioceptive
sensors. The rationale was that for subjects to recognize the
head position at the target angle in the horizontal yaw
plane, mainly proprioceptive information would be infor-
mative. Because both groups improved their accuracy,
appropriate vestibular information was of no further ben-
eWt. One might speculate that the task was simpliWed by
removing dynamic information during target introduction,
leaving the subjects to rely mainly on the static position
sense. These Wndings suggest an interaction between static
and dynamic cues in cervical proprioceptive information.
Such interaction may under other circumstances provide a
hypothetical basis for an internal sensory mismatch of
cervicogenic origin (Brandt and Bronstein 2001; Karlberg
et al. 1996; Malmstrom et al. 2007), analogous with the
mismatch between vestibular dynamic canal and static
otolith information (Kohl 1983).
Some methodological constraints could inXuence the
results and the comparability with other studies. The active
repositioning to each position was repeated three times,
which has been reported to be reliable (Lee et al. 2006;
Swait et al. 2007). More repetitions might have been better
(Pinsault et al. 2008a; Swait et al. 2007), but since the sub-
jects were tested with four diVerent position tests, three rep-
etitions were chosen in order to avoid fatigue and loss of
interest (Pinsault et al. 2008a). When the present study was
designed no information was available about which head
repositioning tests were to be preferred in order to detect
possible deWcits in the bilateral vestibulopathy group.
Therefore, we used several diVerent tests. Kristjansson and
Table 5 Absolute error for 10° target (TAR), 30° target, 30° target with oscillating (osc) movements during introduction and neutral head position
(NHP)
Subjects with bilateral vestibulopathy (BV) are compared to controls. Values are reported in degrees. Mean (Mn), standard deviation (SD), stan-
dard error of the mean (SEM), 95% conWdence interval (CI) and p values are shown
Equal variances assumed (Levene’s test > 0.05) in t test. Uncorrected and corrected p values (adjusting for age and gender eVect; age and gende
r
as covariates) are reported
BV (n= 11) Controls (n= 15) Independent t test
Controls-BV Uncorrected Corrected
Mn (SD) SEM Mn (SD) SEM 95% CI p value p value
10° TAR
Right 8.0 (3.4) 1.0 5.5 (3.7) 1.0 ¡5.2–0.4 0.091 0.058
Left 6.0 (6.8) 2.0 4.5 (2.3) 0.6 ¡5.3–2.5 0.458 0.827
30° TAR
Right 6.3 (4.1) 1.3 6.8 (5.2) 1.3 ¡3.4–4.4 0.800 0.417
Left 5.4 (2.4) 0.7 6.3 (4.3) 1.1 ¡2.1–3.9 0.533 0.448
30° TAR
Right osc 7.3 (4.1) 1.2 6.0 (4.2) 1.1 ¡4.7–2.0 0.426 0.889
Left osc 6.2 (5.2) 1.6 5.5 (3.3) 0.8 ¡4.1–2.7 0.684 0.797
NHP
Right 2.8 (2.5) 0.8 3.9 (1.7) 0.4 ¡0.6–2.7 0.212 0.636
Left 2.7 (1.8) 0.5 2.9 (2.2) 0.6 ¡1.4–1.9 0.794 0.542
Table 6 Absolute error for 30° target, target introduction with no
oscillating head movements compared with oscillation
Subjects with bilateral vestibulopathy (BV) and controls are reported
separately. Mean diVerence with 95% conWdence interval (CI) and
p
values are shown
BV group Controls
Mean diV
(95% CI), p value
Mean diV
(95% CI), p value
30° target right (°) ¡1.0 (¡3.7–1.6), 0.415 0.8 (¡2.6–4.2), 0.620
30° target left (°) ¡0.8 (¡5.0–3.3), 0.671 0.8 (¡2.1–3.7), 0.575
Eur J Appl Physiol (2009) 107:73–81 79
123
Lee with co-workers found NHP to be more sensitive to
detect diVerences between subjects with and without neck
pain (Kristjansson et al. 2003; Lee et al. 2008). Our results,
with tendencies towards diVerences between the groups, for
movements close to the neutral zone (Panjabi 1992)
(Tables 1, 5) also suggest movements close to the neutral
zone to be more sensitive and more susceptible to sensory
disturbances. This might be of importance for the choice of
rehabilitation methods.
NHP was reproduced without any passive repositioning
to refNHP by the tester between each repositioning. Our
procedure diVered thus somewhat from Revel et al. (1991),
but was similar to other authors (Demaille-Wlodyka et al.
2007; Lee et al. 2008; Teng et al. 2007). The repositioning
without adjustments to zero between the trials was made in
order to detect any possible drift, with the overall aim to
detect possible diVerences between the tested groups.
DiVerent error expressions have been evaluated and rec-
ommended (Hill et al. 2009; Lee et al. 2006). A combina-
tion of CE and AE was proposed (Hill et al. 2009), as well
as CE together with VE (Lee et al. 2006). We report all
three, with information about directional error (CE), vari-
ability error (VE) and overall accuracy (AE) in order to
make comparisons with other studies possible.
Age has been demonstrated to inXuence sensorimotor
performance (Heikkila and Wenngren 1998; Vuillerme
et al. 2008) as well as to aVect repositioning tests in a direc-
tion-speciWc manner (Teng et al. 2007). There was an
uneven distribution between men and women in our BV
group and the controls were on average Wve years younger.
When we adjusted statistically for age and gender, one sig-
niWcant diVerence between the groups emerged, with
undershoot (CE) when turning back to centre from right-
ward rotation.
There is presently no golden standard threshold value of
head repositioning tests to discriminate healthy subjects
from subjects with diVerent disorders. Loudon et al. (1997)
found 3–4° diVerences between subjects with whiplash and
healthy controls for 30° target position. Their AE were
closer to the introduced target for both groups in compari-
son with ours (Table 5). They used a cervical range of
motion device that has been found to agree well with the
Zebris device (Malmstrom et al. 2003). Revel et al. (1994)
suggested a threshold value of 4.5° for NHP tests to sepa-
rate subjects with neck pain from neck healthy subjects.
Pinsault et al. (2008b) found no diVerences between a
group of subjects with BV compared with healthy controls
in the NHP-test, but they did Wnd increased AE for non-
traumatic neck pain patients. They presented lower AE and
higher VE values for both the BV group and controls, com-
pared to our results. Their AE and VE values were obtained
from 20 repositionings with the sides collapsed together.
We had movements to the right and left analyzed sepa-
rately, and it was in the side-speciWc analyses that tenden-
cies towards diVerences appeared (Tables 1, 5). Pinsault
et al. (2008b) suggested that the vestibular system is not
involved in the NHP-test, since they found increased AE
for patients with neck pain but not for BV patients. Their
results do reXect the diYculty to discriminate between nor-
mal performance and that of patients with diVerent disabili-
ties. Perhaps could diVerent tests with speciWed speed of the
head turning and with diVerent threshold values further
clarify and identify disability in diVerent conditions. This is
a question for future research.
The validity of our results might be questioned, since we
did not test any patients with neck pain and thus we do not
know if our head repositioning tests can discriminate
between healthy subjects and neck pain patients.
Demaille-Wlodyka et al. (2007) have provided norma-
tive AE values for NHP tests with the Zebris® system.
Despite minor methodological diVerences, comparison of
the two studies indicates that NHP repositioning ability for
the BV group was the same as that of normal performance.
When we compared the AENHP for our subjects to paired
values retrieved from age-matched data (Demaille-
Wlodyka et al. 2007), both our groups had lower AE.
These diVerences can probably be explained by some
diVerences in the procedure or by variability within the
tested groups and focus on the diYculty to compare results
from diVerent studies. Detailed method descriptions, well-
informed participants, larger groups for comparison and
the use of computerized methods, with less dependency on
the human factor, will hopefully in future studies closer
describe the individual accuracy and variability, both
during normal conditions and during diVerent disability
circumstances.
Our subjects with BV performed the head repositioning
test normally, and in comparison with normative values
(Demaille-Wlodyka et al. 2007). The results of the present
study further support previous results (Nakamura and
Bronstein 1995; Pinsault et al. 2008b) and emphasize that
cervical proprioception is suYcient for horizontal head
position perception.
Conclusion
Subjects with bilateral vestibulopathy maintain their ability
to perceive and Wne-tune head on trunk movements in the
horizontal yaw plane when movements are performed at
their own speed. Two possible explanations of this Wnding
are that vestibular information is of less importance for this
task or that cervical somato-sensory input is up-regulated as
a compensatory mechanism after bilateral vestibular loss.
Both hypotheses emphasize the importance of cervical pro-
prioception for head orientation.
80 Eur J Appl Physiol (2009) 107:73–81
123
Acknowledgments Financial support was received from the Skane
County Council’s Research and Development Foundation, the Swed-
ish Research Council, Stockholm, the Crafoord Foundation, Lund and
the Faculty of Medicine, Lund University, Lund, Sweden.
ConXict of interest statement The authors declare that they have no
conXict of interest.
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