BALANCE PROBLEMS WITH PARKINSON’S DISEASE: ARE THEY
E. P. PASMAN,a,bC. D. MURNAGHAN,aB. R. BLOEMb
AND M. G. CARPENTERa*
aSchool of Human Kinetics, The University of British Columbia, Os-
borne Centre Unit I, 6108 Thunderbird Boulevard, V6T 1Z3, Vancou-
ver, BC, Canada
bDepartment of Neurology, Donders Institute for Brain, Cognition and
Behavior, Radboud University Nijmegen Medical Centre, PO Box
9101, 6500 HB Nijmegen, The Netherlands
Abstract—Non-motor symptoms, such as fear of falling and
anxiety, are frequently reported in Parkinson’s disease (PD).
Recent evidence of anxiety and fear directly influencing bal-
ance control in healthy young and older adults, raises the
question whether fear of falling and anxiety also directly
contribute to the balance deficits observed in PD. The goal of
the current study was to examine whether PD patients and
controls responded similarly or differently to experimentally
induced increases in anxiety. For this purpose, 14 PD pa-
tients (tested during a subjective optimal ON state) and 16
healthy age-matched control subjects stood in three condi-
tions of different levels of postural threat: normal threat
(quiet standing at ground level); medium threat (standing at
the edge of a surface elevated to 80 cm); and high threat
(same, but to 160 cm). Outcome measures included mean
position, mean power of frequency (MPF) and root mean
square (RMS) of centre of pressure (COP) displacements in
the anterior-posterior (AP) and medial-lateral (ML) directions.
Physiological and psychosocial measures of fear and anxiety
were also recorded. Increased threat changed postural con-
trol similarly in PD patients and controls; MPF of AP and ML
COP increased and the mean COP position was shifted back-
ward in both groups. These results indicate that during the
ON state, static balance in PD patients and controls is equally
susceptible to the influence of anxiety. Significant correla-
tions observed between COP changes and measures of fear
and anxiety provide evidence to support the proposed neural
links between structures controlling emotion and postural
control. Future studies should further address this issue by
including more severely affected patients, by testing the in-
fluence of dopaminergic medication, by including more anx-
ious patients, and by using dynamic measures of balance.
© 2011 IBRO. Published by Elsevier Ltd.
Elsevier OA license.
Key words: Parkinson’s disease, balance, postural control,
anxiety, fear of falling.
Postural instability is a particularly disabling symptom in
Parkinson’s disease (PD) as it frequently leads to falls and
injuries (Koller et al., 1989; Bloem et al., 2001). Medical
management of postural instability remains difficult (Bloem
and Bhatia, 2004), and development of improved therapies
is hampered by lack of adequate pathophysiological in-
sights. Careful assessment of the characteristics of pos-
tural control in PD is therefore a major issue for this patient
population, as this provides the basis for rational develop-
ment of improved treatment strategies tailored to specific
One way in which postural control is assessed in PD is
to measure the characteristics of postural sway during
periods of quiet stance. Sway is typically assessed by
having subjects stand quietly on a forceplate, which re-
cords ground-reaction forces and moments that can be
used to calculate the centre of pressure (COP), a weighted
average of all forces acting beneath the feet (Winter et al.,
1996). The COP is considered the primary control variable
responsible for restricting natural sway of the body’s centre
of mass (COM) and thus maintain equilibrium. The char-
acteristics of the COP signal are usually quantified in terms
of its mean position, amplitude and frequency of displace-
ments in the anterior-posterior (AP) and medial-lateral
(ML) directions, which are known to be controlled indepen-
dently by the CNS (Winter et al., 1996). Amplitude and
frequency measures are used to describe the oscillatory
nature of the COP signal which reflects the net neuromus-
cular response of the CNS to control the COM. Mean
position of the COP reflects the average vertical projection
of the COM during stance and therefore provides an indi-
rect measure of leaning during stance.
While a number of prior studies have measured the
characteristics of postural sway to investigate quiet stand-
ing performance in PD, the results have been inconsistent.
For example, during quiet standing some investigators
observed PD patients to have larger amplitudes of postural
sway compared to age-matched controls (Mitchell et al.,
1995; Contin et al., 1996; Rocchi et al., 2002; Maurer et al.,
2003; Nardone and Schieppati, 2006; Błaszczyk et al., 2007);
some have found no difference between the groups (Schiep-
pati and Nardone, 1991; Termoz et al., 2008); while another
found smaller postural sway in PD patients (Horak et al.,
1992). While studies have shown the frequency (or veloc-
ity) of COP displacements to be higher in PD patients
compared to elderly controls (Rocchi et al., 2002; Maurer
et al., 2003), the changes in mean position are more
variable; some studies have reported a forward shift in
mean COP position in PD patients compared to elderly
controls (Błaszczyk et al., 2007; Termoz et al., 2008), while
another has reported a more backward shift of mean COP
in PD patients (Schieppati and Nardone, 1991).
*Corresponding author. Tel: ?1-604-822-8614; fax: ?1-604-822-9451.
E-mail address: firstname.lastname@example.org (M. G. Carpenter).
Abbreviations: AP, anterior posterior; COM, centre of mass; COP,
centre of pressure; GSR, galvanic skin response; ML, medial lateral;
MMSE, mini mental state examination; MPF, mean power of fre-
quency; PANAS-X, positive and negative affect schedule– expanded
form; PD, Parkinson’s disease; RMS, root mean square; UPDRS,
unified Parkinson’s disease rating scale.
Neuroscience 177 (2011) 283–291
0306-4522/11© 2011 IBRO. Published by Elsevier Ltd.
Open access under the
Open access under the Elsevier OA license.
The potential origins of balance deficits in PD also
remain largely unclear. Traditionally postural deficits have
been attributed to disrupted dopaminergic pathways in the
basal ganglia specifically responsible for processing motor
commands. However, evidence is beginning to suggest
that balance problems may not be solely attributable to the
result of motor processing deficits in PD (Wright et al.,
2010; Beckley et al., 1993; Brown et al., 2007). Further-
more, while pharmacological and surgical treatments are
highly successful in alleviating motor symptoms such as
bradykinesia, stiffness and tremor, they often provide little
to no improvement to postural control during quiet stance
(Rocchi et al., 2002; Bloem and Bhatia, 2004; Bloem et al.,
1996). As such, attention has now started to shift to con-
sider other non-motor functions within the basal ganglia as
possible contributors to the development of postural defi-
cits in PD.
Of the basal ganglia’s non-motor functions, its role in
emotional processing, has received the least consideration
as a possible contributor to postural control. One of five
parallel circuits within the basal ganglia, the limbic circuit is
thought to be involved in higher-order processing of emo-
tional information, and acts as a gate for widespread
sources of emotional cues. Emotion is also commonly
affected by PD. For example, between 28% and 38% of
PD patients are diagnosed with clinical anxiety disorders
according to Diagnostic and Statistical Manual of Mental
Disorders III-R criteria (Stein et al., 1990; Menza et al.,
1993). Non-clinical anxiety is found in 20–69% of PD
patients (Aarsland et al., 1999; Kulisevsky et al., 2008),
while up to 45% of PD patients have a fear of falling (Bloem
et al., 2001). These rates are significantly higher than
those reported for healthy elderly persons (Lyketsos et al.,
2000; Bloem et al., 2001; Ritchie et al., 2004; Trollor et al.,
2007; Geda et al., 2008). Furthermore, PD patients have
deficits in generating normal physiological and cortical re-
sponses to emotional or threatening stimuli (Yoshimura et
al., 2005; Bowers et al., 2006; Tessitore et al., 2002).
Interconnections between limbic and motor control cir-
cuitry within the basal ganglia, provide the means for the
CNS to shape motor outputs based on the emotional con-
text or meaning of a situation (Nakano, 2000), and may
explain the relationship observed between anxiety and
motor symptom severity in patients with PD (Routh et al.,
1987). However, the question remains whether dysregula-
tion of emotions, such as fear and anxiety, can also con-
tribute to postural deficits associated with PD. The poten-
tial for anxiety to directly influence postural control has
been recently demonstrated in healthy individuals. For
example, studies have used elevated surface heights to
directly investigate the effect of fear and anxiety on pos-
tural control in healthy young and older adult populations.
The results of these studies suggest that standing on an
increased surface height leads to changes in postural con-
trol, including a decrease of the amplitude and an increase
of the frequency of AP COP displacements, as well as a
backward displacement of the mean COP position (Car-
penter et al., 1999, 2001a, 2006; Adkin et al., 2000; Brown
et al., 2006). Whether such mechanisms are also at play in
PD is much less clear. One study found that PD patients do
not employ the same postural strategies as healthy con-
trols when standing at or away from the edge of an ele-
vated surface (Brown et al., 2007). However, this study
had several possible drawbacks: standing was measured
for only very short time periods (15 s); changes in anxiety
and fear were not verified experimentally; and it was step
restriction as opposed to surface height that was used to
manipulate postural threat.
Therefore, the aim of this study was to examine
whether PD patients and controls would respond similarly
to increases in postural threat. Based on earlier work
(Brown et al., 2007), we hypothesized that PD patients
would not utilize the same postural strategies as healthy
controls when standing on elevated surface heights.
Fourteen subjects with PD and 16 healthy age-matched control
subjects participated in the study (Tables 1 and 2). Each participant
provided written informed consent prior to testing. The Hoehn and
Yahr scale and motor examination subscale of the unified Parkin-
of motor symptoms in PD patients. All participants completed a fall
history and medical history survey, the mini mental state examination
(MMSE) (Folstein et al., 1975), and the frontal assessment battery
(Dubois et al., 2000). Because medication generally has little effect
on postural control during quiet stance (Rocchi et al., 2002; Bloem
and Bhatia, 2004; Bloem et al., 1996), all PD patients were examined
during their subjectively best ON clinical condition. Testing was timed
to coincide with the expected time of each patient’s subjectively best
clinical condition, approximately 1 h after intake of their regular Par-
kinson medication (Tables 1 and 2). Participants were excluded if
they had a medical condition other than PD that interfered with their
balance, or had an MMSE score ?24. Subjects were also excluded
if they had an extreme fear of heights, a history of anxiety disorders
or were taking any anti-anxiety medications. PD patients were ex-
cluded if they had a neurosurgical procedure for their PD, or when
neurological examinations showed considerable postural tremor or
significant dyskinesias that would influence the COP recordings. All
experimental procedures were approved by the UBC Clinical Re-
search Ethics Board.
Subjects stood quietly in stocking feet on a forceplate (model
#k00407, Bertec, USA) covered by a non-compliant rubber mat (0.5
cm thick) for a period of 120 s in four different conditions. The first
condition was standing on ground level (normal condition), with the
top surface of the forceplate located 9 cm above the ground. The
second was a reduced threat condition which involved standing on
ground level with additional safety features in place. However, this
condition failed to elicit desired effects on reducing anxiety and
increasing confidence in either group and was thus excluded from
further analysis. The third condition was standing at the edge of a
hydraulic platform elevated 80 cm above the ground (medium threat
condition). The fourth was standing at the edge of the hydraulic
platform elevated 160 cm above the ground (high threat condition).
To ensure the safety of participants during the trials on the hydraulic
platform, participants wore a safety harness which was securely
fastened with rope to a support beam in a manner that did not
interfere with their postural control. In all conditions a spotter stood
behind the participants during the trial. The participants stood with
their eyes open, arms hanging loosely by their sides and feet placed
E. P. Pasman et al. / Neuroscience 177 (2011) 283–291284
shoulder width apart during each trial. The foot position of the par-
the same foot position in every trial. Participants were instructed to
focus during the standing trial on a visual target placed at eye level
approximately 3 m in front of them. A practice trial on ground level
was performed first to allow participants to become familiarized with
the procedures and remove any potential first trial effects (Adkin et
standing trial in the normal condition, followed by the reduced threat,
medium threat and high threat condition, with a few minutes of
seated rest in between each standing condition. The effect of pos-
tural threat on postural control is known to be influenced by order,
with greater postural changes observed when participants stand in
increasingly threatening, compared to less threatening, conditions
(Adkin et al., 2000). Based on this knowledge, the four conditions
were presented in a fixed order across participants, to maximize the
potential effect of threat, and thus provide the greatest opportunity to
observe potential interactions with PD. Randomization would likely
nullify the effect of threat on postural control, making potential inter-
actions between groups and threat more difficult to discern.
Several questionnaires were used to assess levels of anxiety, fear
and balance confidence prior to testing, as well as before and after
each standing trial. Prior to performing the practice trial, partici-
pants filled in the trait section of the state and trait anxiety inven-
tory which uses a 4 point scale (from 1 (almost never) to 4 (almost
always)) to rate 20 different statements referring to individual
differences in the frequency and intensity with which anxiety man-
Table 1. Baseline subject characteristics
Number of women (%)
Fear of falling
Fear of heights
Mini mental state examination
Frontal assessment battery
Duration of disease (years)
Hoehn and Yahr score
UPDRS motor examination score
Data are displayed as mean (standard deviation) or as the number of persons (percentage between parentheses). NS, not significant; S, significant.
Table 2. Demographic data PD patients
Maximum ABC scale score is 100, maximum trait anxiety score is 80, maximum UPDRS motor score is 108, maximum Hoehn and Yahr score
E. P. Pasman et al. / Neuroscience 177 (2011) 283–291285
ifests itself over time (Barnes et al., 2002). Prior to each standing
trial, participants rated how confident they were that they could
maintain their balance and avoid a fall during the upcoming bal-
ance task on a scale from 0% (not confident at all) to 100%
(completely confident). After each standing trial, participants rated
how stable and how fearful of falling they felt during the trial, both
on a scale from 0% (i.e. not stable/not fearful of falling) to 100%
(i.e. completely stable/fearful of falling) (Hauck et al., 2008). After
each trial, participants also filled in the state anxiety questionnaire,
which consists of 16 items rated on a scale from 1 (didn’t feel at
all) to 9 (felt this extremely) (Hauck et al., 2008) and the positive
and negative affect schedule-expanded form (PANAS-X) fear sub-
scale, where participants indicate the extent to which they feel (on
a scale from 1 (not at all) to 5 (extremely)) about six words that
describe different feelings and emotions (Watson and Clark,
During the trials, participants’ galvanic skin response (GSR)
and ground reaction forces and moments were also recorded.
GSR, a measure of physiological arousal, was recorded from
electrodes placed on the thenar and hypothenar eminence of the
participant’s non-dominant hand (Critchley, 2002). GSR measures
were recorded at a sampling rate of 1 kHz and were smoothed
off-line at a time constant of 0.2 s, prior to calculating the mean
GSR over the entire 120 s trial. The mean GSR for each trial was
normalized to the values recorded during the practice trial. Ground
reaction forces and moments measured from the forceplate on
which the participants stood were sampled at 100 Hz and low pass
filtered offline using a 5 Hz dual-pass Butterworth filter, prior to
calculating the COP in the AP and ML direction. The mean COP
in the AP and ML directions was determined and removed from
the signal prior to calculating the root mean square (RMS) and the
mean power of frequency (MPF) of COP displacements.
Independent T-tests were performed to compare baseline clinical
measures between controls and PD patients (Table 1). All depen-
dent measures were analyzed using a 2?3 between and within
subject analysis of variance with threat (normal, medium and high)
and group (controls and PD) as independent variables. Assump-
tions of normality and homogeneity of variances were examined
and met across most dependent measures, variables and exper-
imental conditions. Tests of assumptions were based on inspec-
tion of histograms and box-plots, and statistical tests of homoge-
neity. Levine’s tests demonstrated equality of variances across
groups for all measures (P?0.05). In the few cases where Box’s
M tests of equality of co-variance matrices (P?0.001) and/or
Mauchly’s tests of sphericity (P?0.05) were significant, the Green-
house–Gueisser ? statistic was used. An overall ??0.05 was used
for all statistical comparisons. In cases of significant main and
interaction effects, post hoc comparisons were performed after
adjusting for multiple comparisons using a Bonferroni correction
(adjusted level of significance?0.017). Differences between high
threat and normal threat conditions were also calculated and used
to examine associations between changes in psycho-social and
GSR measures with changes in postural control using Pearson
product moment correlations (P?0.05).
Manipulation of postural threat via changes in surface
height resulted in significant changes in physiological and
psychosocial indicators of arousal, anxiety and fear in both
groups. There was a significant main effect of threat on the
mean GSR level (F(1.664,46.580)?18.696, P?0.001), with
higher GSR levels observed in the medium and high threat
conditions compared to the normal condition. A significant
main effect of threat was observed for state-anxiety
(F(2,56)?10.626, P?0.001), fear (F(1.185,33.191)?13.382,
P?0.001), fear of falling (F(1.972,55.229)?5.10, P?0.010),
balance confidence (F(1.275,35.713)?5.324, P?0.02) and
perceived stability (F(2,56)?9.626, P?0.001). Significantly
higher scores of state-anxiety and fear were observed in
the high threat condition compared to the normal and
medium threat condition. Fear of falling for the high threat
condition was significantly higher than for the normal con-
dition. Balance confidence was significantly lower in the
medium and high threat condition compared to the normal
condition. Perceived stability was also significantly lower in
the high threat condition compared to the normal condition,
and medium threat condition. There was no significant
main effect of group or interaction between threat and
group on GSR or psychosocial measures (Fig. 1).
Postural threat also had a significant influence on COP
measures in both groups (Fig. 2). There was a significant
main effect of threat on the mean position of AP-COP
(F(1.579,44.202)?54.653, P?0.001). The mean position of
AP-COP was shifted significantly backwards (away from
the edge) in the medium and high threat conditions com-
pared to the normal condition, and in the high threat com-
pared to medium threat condition. There was also a sig-
nificant main effect of threat on the MPF of COP in the
AP (F(1.515,42.425)?14.053, P?0.001) and ML direction
(F(2,56)?3.507, P?0.037). AP-MPF in the medium and
high threat conditions was significantly higher than in the
normal condition, while there was a trend towards higher
ML-MPF in the high threat condition than in the normal
condition (P?0.031). There was no significant main effect
of threat on RMS of COP in the AP (F(2,56)?1.494,
P?0.233) or ML direction (F(1.914,53.592)?0.058, P?0.938).
For all COP measures there was no main effect of group or
interaction between threat and group (Fig. 3).
Across both groups, there was a significant positive
correlation between changes in total anxiety and changes
in MPF of COP in the AP (r?.391, P?0.032) and ML
directions (r?.424, P?0.019). Likewise, there was a sig-
nificant positive correlation between changes in the
PANAS-X fear subscale and changes in RMS of COP in
the AP direction (r?.441, P?0.015). No psychosocial or
GSR changes were correlated to changes in mean COP
Postural threat influenced balance control in both PD
patients and controls
The aim of this study was to examine whether patients and
controls responded similarly to increases in postural threat.
Brown and colleagues investigated whether PD patients
alter their postural control of quiet standing in reaction to
changes in environmental context (postural threat). They
measured quiet standing in a low threat condition (0.6 m
height with a wooden platform in front of the hydraulic lift to
provide an opportunity to step forward) and a high threat
condition (0.6 m height with the wooden platform re-
moved). The results showed that PD patients manifested
no changes in postural control during quiet standing with
E. P. Pasman et al. / Neuroscience 177 (2011) 283–291286
heightened postural threat, while controls showed a signif-
icant posterior shift of mean position of AP-COP and sig-
nificant reduction in RMS amplitude of COP displace-
ments. The authors concluded that PD patients have def-
icits in context-dependent regulation of quiet standing
(Brown et al., 2007). However, these results are inconsis-
tent with the current observations of a posterior shift in
mean position of AP-COP and increased MPF in the AP
and ML direction in both PD patients and controls. Indeed,
the current results indicate that PD patients can react to
changes in threat level similar to controls. Although patient
characteristics, including mean disease duration, the
range in UPDRS motor scores and medications were very
similar between the current study and that of Brown and
colleagues, other differences are noteworthy. One impor-
tant difference between the studies is that Brown and
colleagues actually used step restriction, instead of sur-
face height, to increase postural threat. It has been shown
that surface height influences balance control during quiet
stance independent of step restriction (Carpenter et al.,
1999). Furthermore, Brown and colleagues did not mea-
sure psychosocial or physiological indicators of anxiety or
fear, in order to confirm the extent to which the manipula-
tion of step restriction leads to changes in fear or anxiety.
In contrast, the current study demonstrated that the ma-
nipulations of surface height were accompanied by signif-
icant changes in self-reported ratings of state anxiety, fear,
balance confidence and perceived stability in both PD
patients and controls. Furthermore changes in state anxi-
ety and fear were found to be significantly correlated with
changes in postural control across groups. Another impor-
tant difference between studies was the time period used
to collect COP measures during quiet stance. Brown and
colleagues used a sampling duration of only 15 s, which is
possibly too short to record reliable amplitude and fre-
quency measures of postural control during quiet stance
(Carpenter et al., 2001b). In contrast, the current study
sampled COP measures over 120 s of quiet stance, which
exceeds the minimum time period required to ensure reli-
able and accurate measures of amplitude and frequency of
COP displacements (Carpenter et al., 2001b).
The significant relationships observed between fear
and anxiety on postural control adds further support to the
proposed neural link between areas of the brain controlling
emotion, and areas responsible for balance control in hu-
mans (Balaban and Thayer, 2001). In particular, the
amygdala and associated limbic structures are central to
the acquisition, modulation and expression of emotions,
such as fear and anxiety, and have widespread efferent
connections to areas involved in posture, including vestib-
Fig. 1. Physiological and psychosocial anxiety measures. Bar graphs of population means and standard errors of mean GSR level (A), PANAS-X fear
subscale score (B), fear of falling (C), state-anxiety questionnaire score (D), balance confidence (E) and perceived stability (F), with black bars
indicating controls and white bars indicating PD patients. Asterisks represent significant differences in post-hoc comparisons between levels of threat
E. P. Pasman et al. / Neuroscience 177 (2011) 283–291287
ular nuclei, the reticular formation, and nuclei within the
basal ganglia and nucleus accumbens (Cardinal et al.,
2002; Balaban and Thayer, 2001).
Due to study limitations, the current results are unable to
clarify the basal ganglia’s role in mediating the effects of
anxiety and fear on postural control. One such limitation was
that participants were tested after they had taken their normal
doses of Parkinson medication. Although dopaminergic med-
particularly during quiet stance (Rocchi et al., 2002; Bloem
and Bhatia, 2004; Bloem et al., 1996), it may offer significant
improvements to anxiety and emotional processing deficits in
PD (Witjas et al., 2002; Maricle et al., 1995a,b; Tessitore et
al., 2002). Therefore, future studies need to include PD pa-
tients both ON medication (ideally after a supramaximal
levodopa dose, to ensure an optimal and consistent ON
phase throughout the experiment) and OFF medication, in
order to ascertain the basal ganglia’s role in mediating anxi-
ety-related changes in postural control.
Another limitation of the study was that subjects were
extreme fear of heights, and/or treatment with anti-anxiety
medications. The exclusion of those with anxiety disorders
and extreme fear of heights was justified on ethical grounds,
to avoid placing patients in threatening conditions that could
potentially trigger an anxiety attack or phobic reactions. Sub-
jects taking anti-anxiety medication were excluded for meth-
odological reasons as the medication would likely mask any
normal anxiety response to the threat of standing on elevated
surfaces. However, we realize that this may have impacted
our ability to detect differences between groups, and thus,
limited any insight into how the basal ganglia may contribute
to anxiety-related effects on postural control. It also limits the
ability to generalize the current results to the significant num-
ber of patients that suffer from clinical and non-clinical anxiety
(Stein et al., 1990; Menza et al., 1993; Aarsland et al., 1999;
Kulisevsky et al., 2008). Therefore, further studies should be
done to investigate the influence of anxiety and fear on the
postural control of PD patients with known anxiety.
A third limitation is that subjects included in this
study were relatively well functioning and showed little
evidence of postural deficits during clinical examination
and fall history. Although nine of the subjects scored
abnormally on the clinical postural test, only two had a
history of falls, and both of these subjects responded to
the changes in height in the same way as the others.
Irrespectively, there are still questions regarding whether
subjects with more severe motor and postural deficits
would show greater differences in postural control com-
pared to controls, and whether they may respond differ-
ently to changes in postural threat.
No main effect of PD on postural control measures
In this study, no significant differences were observed
between PD patients and controls in terms of amplitude,
frequency, or mean position of COP. This result provides
further evidence in support of prior studies that have re-
ported no significant differences in COP measures be-
tween PD patients and controls during quiet stance (Schi-
Fig. 2. Single subject COP data. Single subject recordings of COP displacements during 120 s standing trials under conditions of normal threat (left),
medium threat (middle) and high threat (right) conditions. The illustration purposes, origin of the axes have been normalized to the mean position of
the normal threat condition with negative values on the x and y axis representing leftward and backward directions respectively.
E. P. Pasman et al. / Neuroscience 177 (2011) 283–291288
eppati and Nardone, 1991; Termoz et al., 2008). These
findings contradict others that have reported the effects of
PD on COP amplitude (Horak et al., 1992; Mitchell et al.,
1995; Contin et al., 1996; Rocchi et al., 2002; Maurer et
al., 2003; Nardone and Schieppati, 2006; Błaszczyk et
al., 2007), frequency, (Rocchi et al., 2002; Maurer et al.,
2003), or mean position of COP (Schieppati and Nar-
done, 1991; Błaszczyk et al., 2007; Termoz et al., 2008).
Differences between the current study and previous work
are not likely related to differences in disease severity of
patients, as the UPDRS and Hoehn and Yahr scores were
similar to those reported in prior studies. Therefore, likely
sources of variation may be attributed to differences in
experimental protocols, including instruction, sample dura-
tion and analysis, timing and dose of medication, or the
presence of other co-morbidities (including anxiety symp-
Relevance of the findings to a clinical setting
Despite the limitations described above, the results of
this study show that the postural control of quiet stand-
ing in healthy elderly control subjects and PD patients on
medication is equally susceptible to the influence of
anxiety. Given the high prevalence of anxiety and fear of
falling in PD patients, it should be considered a factor
when interpreting balance assessments in this patient
population. This should be done especially if compari-
sons are made with healthy elderly control subjects, in
whom the prevalence of anxiety and fear is lower than in
Evidence that sources of anxiety can influence balance
in older healthy adults (Carpenter et al., 1999, 2006; Brown
et al., 2006; Geh et al., 2010), as well as PD patients, also
highlights the need for clinicians to account for other po-
tential sources of anxiety or fear that could either mask or
mimic a potential balance deficit. Potential sources of anx-
iety include anxiogenic or anxiolytic medications, clinical or
non-clinical anxiety disorders, and social anxiety related to
the prospect of being negatively evaluated by the clinician
(Geh et al., 2010).
In summary, the results of this study indicate that static
balance in PD patients and healthy elderly controls is
equally susceptible to the influence of anxiety. Future
studies could further address this issue by including
more severely affected patients both ON and OFF do-
paminergic medication, more anxious patients, or by
using dynamic measures of balance.
Acknowledgments—We gratefully acknowledge the funding pro-
vided by Prinses Beatrix Fonds, Parkinson Patiënten Vereniging
Fig. 3. COP summary measures. Bar graphs of population means and standard errors of AP mean (A), MPF (B) and RMS (C) of COP, and ML MPF
(D) and RMS (E) of COP, with black bars indicating controls and white bars indicating PD patients. Asterisks represent significant differences in
post-hoc comparisons between levels of threat (P?0.017).
E. P. Pasman et al. / Neuroscience 177 (2011) 283–291 289
Nederland, Stichting Nijmeegs Universiteitsfonds and NSERC.
Prof. Bloem was supported by an NWO VIDI grant (# 016.076.
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(Accepted 25 December 2010)
(Available online 8 January 2011)
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