Parkinsonism and Related Disorders 25 (2016) 72e77

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Parkinsonism and Related Disorders

journal homepage: www.elsevier.com/locate/parkreldis

Postural sensory correlates of freezing of gait in Parkinson's disease

Young Eun Huh a, Seonhong Hwang b, Keehoon Kim b, Won-Ho Chung c,
Jinyoung Youn d, e, Jin Whan Cho d, e, *
a
Department of Neurology, CHA Bundang Medical Center, CHA University, Seongnam, South Korea
b
Center for Robotics Research, Korea Institute of Science and Technology, Seoul, South Korea
c
Department of Otolaryngology, Head and Neck Surgery, Sungkyunkwan University School of Medicine, Samsung Medical Center, Seoul, South Korea
d
Department of Neurology, Sungkyunkwan University School of Medicine, Samsung Medical Center, Seoul, South Korea
e
Neuroscience Center, Samsung Medical Center, Seoul, South Korea

a r t i c l e i n f o a b s t r a c t

Article history: Introduction: To elucidate the unique patterns of postural sensory deficits contributing to freezing of gait
Received 7 December 2015 (FOG) in patients with Parkinson's disease (PD) and to identify postural sensory modalities that correlate
Received in revised form with FOG severity.
27 January 2016
Methods: Twenty-five PD patients with FOG, 22 PD patients without FOG, and 26 age-matched controls
Accepted 1 February 2016
were evaluated using a sensory organization test and clinical measures including the Unified Parkinson's
Disease Rating Scale motor score, Montreal Cognitive Assessment, Frontal Assessment Battery, Activities-
Keywords:
specific Balance Confidence, Beck Anxiety Inventory, Beck Depression Inventory, and Berg Balance Scale.
Parkinson's disease
Freezing of gait
Multivariable logistic regression analysis was performed for posturographic parameters and possible
Postural sensory deficits confounders to determine postural sensory contributors to FOG. We also correlated FOG severity,
Vestibular impairment measured using a New Freezing of Gait Questionnaire, with posturographic parameters.
Results: PD patients with FOG showed worse postural sensory processing compared with those without
FOG. In particular, the inability to use the vestibular information (odds ratio [OR] 1.447; 95% confidential
interval [CI]: 1.120, 1.869) and poor control over the perturbed somatosensory inputs (OR 2.904; 95% CI:
1.028, 8.202) significantly contributed to FOG. Among PD patients with FOG, FOG severity was correlated
with higher reliance on visual information (r ¼ 0.432, p ¼ 0.039).
Conclusions: Postural sensory deficits involving specific sensory modalities are strongly associated with
FOG. Quantitative measurement of postural sensory deficits in PD patients with FOG may provide a
better understanding of pathomechanisms of FOG and increase the efficacy of sensory cueing strategies
for alleviating FOG, by more accurately identifying suitable patients for rehabilitative therapies.
© 2016 Elsevier Ltd. All rights reserved.

1. Introduction with FOG, reflecting its complex pathomechanism [1e3].

Freezing of gait (FOG) is characterized by an episodic inability to
generate effective stepping despite intention to walk [1]. It is a
devastating condition in patients with Parkinson's disease (PD), as
it causes falls and diminishes mobility and quality of life [1]. Several
factors, including disease severity, cognitive dysfunction, attention
deficits, emotional state, and postural instability, are associated
* Corresponding author. Department of Neurology, Sungkyunkwan University
School of Medicine, Neuroscience Center, Samsung Medical Center, 81 Irwon-Ro
Gangnam-gu, Seoul, 135-710, South Korea.
E-mail addresses: nana1880@hanmail.net (Y.E. Huh), sh@kist.re.kr (S. Hwang),
khk@kist.re.kr (K. Kim), wonho.chung@samsung.com (W.-H. Chung), genian.
youn@samsung.com (J. Youn), jinwhan.cho@samsung.com (J.W. Cho).
PD patients with FOG also exhibit deficits in sensory processing
[4e6]. During normal locomotion, sensory signals from visual,
vestibular, and somatosensory systems are integrated via central
neural networks and provide real-time information used as refer-
ences for cognitive, emotional, and automatic locomotor processes
[7]. Accordingly, the inability to integrate postural sensory inputs
may contribute to the generation of FOG [7]. Indeed, FOG can be
provoked under sensory conflicting situations in which balance is
challenged [1] and also alleviated by various sensory cues [1,8,9].
However, little is known about how postural sensory deficits are
implicated to pathomechanisms of FOG.
We aimed to characterize postural sensory deficits in PD pa-
tients with FOG and to determine specific patterns of postural
sensory deficits that contribute to FOG. Quantitative

http://dx.doi.org/10.1016/j.parkreldis.2016.02.004
1353-8020/© 2016 Elsevier Ltd. All rights reserved.
 Y.E. Huh et al. / Parkinsonism and Related Disorders 25 (2016) 72e77
posturographic measures were compared between PD patients
with and without FOG using a sensory organization test (SOT). We
also identified postural sensory modalities associated with the
severity of FOG.
2. Methods
2.1. Subjects
We recruited 47 patients with idiopathic PD and 26 age-
matched healthy controls through the Movement Disorders Clinic
of Samsung Medical Center. A diagnosis of idiopathic PD was made
by a specialist experienced in movement disorders (J.W.C) based on
UK Parkinson's Disease Society Brain Bank criteria. All patients
were taking levodopa in combination with dopamine agonist and
experienced levodopa-related motor fluctuations. Subjects were
excluded if they could not safely stand unaided, or had a history of
falls in the last 12 months, dementia, visual disturbances, clinical
signs of disorders affecting proprioception, musculoskeletal prob-
lems, orthostatic hypotension, or neurosurgical interventions.
Subjects were also excluded if they had a history or clinical signs of
vestibular diseases, including the presence of spontaneous or head-
shaking nystagmus or corrective saccades during head impulse
testing. Motor disability was assessed using the Unified Parkinson's
Disease Rating Scale motor score (UPDRS-III). For clinical balance
measurement, we used the Berg Balance Scale (BBS), a 56-point
scale in which lower scores indicate worse balance [10]. Global
cognitive and executive functions were tested using Montreal
Cognitive Assessment (MOCA) and Frontal Assessment Battery
(FAB), respectively. The New Freezing of Gait Questionnaire
(NFOGQ) was used to evaluate the presence and severity of FOG
[11]. The Activities-specific Balance Confidence (ABC) scale
(0e100%) was used to estimate fear of falling (FOF) by measuring
confidence in maintaining balance while performing various
ambulatory activities [10,12]. Lower scores indicate greater FOF. All
subjects completed the Beck Depression Inventory (BDI) and Beck
Anxiety Inventory (BAI). Clinical and neurological examinations
and posturography were performed during the morning off-
medication, at least 12 h after withholding anti-parkinsonian
medications.
Patients were assigned to PD patients with FOG (PD-FOG) if they
experienced FOG at least once during the past month based on
NFOGQ item 1, and one or more FOG episodes were provoked and
detected by two experienced movement specialists (Y.E.H. and
J.W.C.) during experiments. FOG was elicited using a turning-in-
place task in which patients were asked to make tight and rapid
360 turns to the left or right for 2 min, immediately before pos-
turography assessment [13,14]. All PD-FOG showed worse freezing
during the off-medication state, and no PD patients without FOG
(PD-noFOG) reported either self-assessed or experimentally pro-
voked FOG episodes. PD-FOG and PD-noFOG were matched for age
and off Hoehn and Yahr stage, which ranged from 2 to 3.
Written informed consent was obtained from each subject and
the study protocol was approved by the Institutional Review Board
of Samsung Medical Center.
2.2. Posturography
Postural sensory deficits were assessed using the SOT protocol
of a computerized dynamic posturography system (EquiTest®;
NeuroCom International, Clackamas, OR, USA) [15], which was
equipped with a force plate enclosed by a visual surround. During
the SOT, subjects stood on the force plate from which the position of
their center of pressure was recorded at a sampling rate of 100 Hz.
Digitized center of pressure data were automatically converted into
73
center of gravity sway and analyzed using an arithmetic algorithm
provided by the EquiTest® system. The force plate and visual sur-
round were fixed or programmed to revolve in reference to sub-
ject's sways in an anterior-posterior direction. By manipulating
fixed/sway-referenced and eye open/closed conditions, visual
and/or somatosensory inputs were distorted or eliminated. The SOT
protocol consisted of six conditions (Fig. 1A). Static balance mea-
sures were obtained from condition 1 in which all sensory sources
were available. In conditions 2 and 3, visual inputs were absent and
distorted, respectively. In the last three conditions, somatosensory
inputs were distorted, while visual inputs were available (condition
4), absent (condition 5), or inaccurate (condition 6).
All participants were outfitted with a safety harness and stood
barefoot at a standardized stance width based on their body height.
They were instructed to remain as still as possible in an upright
posture during each condition, which was composed of three
repeated 20-s trials. A fall was noted when subjects swayed beyond
their limit of stability, requiring a corrective step or assistance.
2.3. Balance measurements
To assess postural stability, an equilibrium score was obtained
from each SOT trial, by comparing the maximum angle of center of
gravity sway in an anterior-posterior direction with the theoretical
limit of stability which was assumed to be 12.5 (Fig. 1B) [15].
Equilibrium scores ranged from 0% to 100%, with higher scores
indicating better ability to maintain balance and 0% indicating a fall.
Averaged equilibrium scores of three trials (ESs) from each SOT
condition were used to assess postural stability.
Sensory ratios (SRs) were calculated to measure the contribu-
tion of each sensory input to postural balance [15]. The ability to use
somatosensory information (SR-SOM), visual information (SR-VIS),
and vestibular information (SR-VEST) were estimated as ratios
between the ES of condition 2 (ES2) and ES of condition 1 (ES1),
between the ES of condition 4 (ES4) and ES1, and between the ES of
condition 5 (ES5) and ES1, respectively. Lower SRs indicated a
poorer ability to use relevant sensory information to maintain
balance. Visual preference (SR-VISPREF) was defined as a ratio of
the sum of the ES of condition 3 (ES3) and the ES of condition 6
(ES6) to the sum of ES2 and ES5. Lower SR-VISPREFs indicated
higher dependency on visual information, even if inaccurate. The
ability to manage distorted somatosensory inputs (SR-MANSOM)
was calculated by dividing the sum of ESs from sway-referenced
plate conditions (ES4 þ ES5 þ ES6) by that from fixed plate con-
ditions (ES1 þ ES2 þ ES3) [16,17].
2.4. Statistical analysis
To assess overall differences between groups in demographic,
clinical, and posturographic variables, KruskaleWallis or Man-
neWhitney U tests, where appropriate, were performed for
continuous data, as normal distributions could not be assumed for
most variables. Significant main effects of group were further
examined by post hoc analysis with Tukey's tests using ranked data.
c2-tests were used to analyze categorical data. To identify postural
sensory modalities contributing to FOG, we conducted a multivar-
iable multinomial logistic regression analysis for all SR values with
adjustment for clinical variables that differed between groups with
p < 0.2. Variance inflation factors (VIFs) were estimated for each
variable entering the multivariable model. Variables with a VIF  10
were considered to have a high level of multi-collinearity and
omitted from the model. VIFs of remaining variables were recal-
culated to ensure an independent association with FOG. To inves-
tigate correlations between the severity of FOG and each postural
sensory modality, Spearman partial correlations were performed
74 Y.E. Huh et al. / Parkinsonism and Related Disorders 25 (2016) 72e77

Fig. 1. Schematic diagram of the sensory organization test. (A) Six conditions of the sensory organization test. Symbols (eye, inner ear, and foot) denote the visual, vestibular, and
somatosensory inputs, respectively. (B) Equation for calculating the equilibrium score (ES). q, the maximum angle of center of gravity sway in an anterior-posterior direction. Images
courtesy of Natus Medical Incorporated.

between NFOGQ scores and SR values, controlling for clinical var- p ¼ 0.980; BDI: p ¼ 0.985).
iables that significantly correlated with NFOGQ scores or SR values
as determined by Spearman correlations. 3.2. Posturographic data

3. Results
3.1. Clinical characteristics
Demographic and clinical characteristics of subjects are shown
in Table 1. Subject groups were similar in terms of age, gender, years
of education, and MOCA and FAB scores. PD-FOG and PD-noFOG
showed equivalent disease duration, Hoehn and Yahr stage, fre-
quency of motor subtype, and levodopa equivalent daily dose. PD-
FOG had lower BBS and ABC scores than PD-noFOG (BBS: p ¼ 0.032;
ABC: p ¼ 0.002) and controls (BBS: p < 0.001; ABC: p < 0.001). PD-
noFOG showed lower BBS (p < 0.001) and ABC (p < 0.001) scores
than controls. PD-FOG and PD-noFOG had higher UPDRS-III, BAI,
and BDI scores than controls, with no significant differences be-
tween the two patient groups (UPDRS-III: p ¼ 0.780; BAI:
Compared with controls, PD-FOG showed lower ESs for most
SOT conditions, except condition 1 (ES2: p ¼ 0.014; ES3: p ¼ 0.011;
ES4: p < 0.001; ES5: p < 0.001; ES6: p < 0.001) (Fig. 2A and
Supplemental Table 1). Compared with PD-noFOG, PD-FOG
exhibited lower ESs for sway-referenced plate conditions, including
ES4 (p ¼ 0.003), ES5 (p < 0.001), and ES6 (p < 0.001). There were no
significant differences in ESs for any SOT condition between PD-
noFOG and controls.
Sensory analysis showed that PD-FOG had more difficulty using
visual (SR-VIS: p ¼ 0.002 vs. PD-noFOG, p < 0.001 vs. controls) and
vestibular (SR-VEST: p < 0.001 vs. PD-noFOG, p < 0.001 vs. controls)
information, and managing distorted somatosensory inputs (SR-
MANSOM: p < 0.001 vs. PD-noFOG, p < 0.001 vs. controls) to ensure
postural balance compared with PD-noFOG and controls (Fig. 2B
and Supplemental Table 1). No SR values differed significantly

Table 1
Demographic and clinical characteristics of subjects.

PD-FOG (n ¼ 25) PD-noFOG (n ¼ 22) Control (n ¼ 26) pa

Age (years) 64.0 (58.5e69.5) 64.5 (61.0e67.8) 64.0 (62.0e66.0) 0.890

Gender (M/F) 13/12 13/9 13/13 0.664
Education (years) 12.0 (12.0e16.0) 12.0 (9.0e16.0) 12.0 (12.0e16.0) 0.567
Disease duration (years) 10.0 (8.0e12.0) 9.0 (7.8e10.3) e 0.211
Hoehn and Yahr stage 2.5 (2.5e3.0) 2.5 (2.0e3.0) e 0.203
UPDRS-III 35.0 (33.0e38.3) 36.0 (31.5e37.3) 0 (0e2.0) <0.001b
PD motor subtypes (PIGD/TD) 15/10 11/11 e 0.564
NFOGQ 12.0 (10.5e18.5) 0 e e
BBS 47.0 (45.0e52.0) 50.0 (48.8e51.3) 56.0 (54.3e56.0) <0.001b,c
MOCA 28.0 (26.0e29.0) 26.5 (25.8e28.0) 28.0 (26.3e29.0) 0.416
FAB 16.0 (14.0e17.0) 16.0 (15.0e17.0) 16.0 (16.0e17.0) 0.342
ABC 75.6 (63.4e85.6) 89.1 (79.1e96.3) 98.4 (97.5e99.4) <0.001b,c
BAI 7.0 (3.0e14.0) 5.0 (3.0e12.3) 1.0 (0e2.0) <0.001b
BDI 8.0 (5.5e15.5) 10.0 (3.5e14.5) 2.0 (0e4.8) <0.001b
LEDD (mg) 768.5 (577.0e901.9) 655.0 (392.3e807.8) e 0.176
Height (m) 1.6 (1.5e1.7) 1.6 (1.5e1.7) 1.6 (1.5e1.7) 0.659
BMI (kg/m2) 23.5 (21.4e26.0) 23.3 (21.1e25.8) 23.7 (21.6e26.4) 0.744

Data are shown as median (25the75th quartiles) unless otherwise noted.

PD-FOG, Parkinson's disease patients with freezing of gait; PD-noFOG, Parkinson's disease patients without freezing of gait; UPDRS-III, Unified Parkinson's Disease Rating Scale
motor score; PD, Parkinson's disease; PIGD, postural instability and gait disturbance; TD, tremor dominant; NFOGQ, New Freezing of Gait Questionnaire; BBS, Berg Balance
Scale; MOCA, Montreal Cognitive Assessment; FAB, Frontal Assessment Battery; ABC, Activities-specific Balance Confidence; BAI, Beck Anxiety Inventory; BDI, Beck Depression
Inventory; LEDD, Levodopa equivalent daily dose; BMI, Body mass index.
a
Based on KruskaleWallis, ManneWhitney U, or c2-tests, as appropriate.
b
Post hoc analysis with Tukey's tests using ranked data: PD-FOG or PD-noFOG vs control.
c
Post hoc analysis with Tukey's tests using ranked data: PD-FOG vs PD-noFOG.
 Y.E. Huh et al. / Parkinsonism and Related Disorders 25 (2016) 72e77 75

Fig. 2. Comparison of posturographic data between subject groups. Boxplots of (A) the equilibrium scores and (B) sensory ratios for PD-FOG, PD-noFOG, and control individuals. The
lower and upper limits of the boxes delineate the 25th and 75th quartile values, respectively. The lines inside the boxes represent the median, and the whiskers show the 5th and
95th percentiles. *p < 0.05, **p < 0.01. PD-FOG, Parkinson's disease patients with freezing of gait; PD-noFOG, Parkinson's disease patients without freezing of gait; C1-6, conditions
1e6; SR-SOM, ability to use somatosensory information; SR-VIS, ability to use visual information; SR-VEST, ability to use vestibular information; SR-VISPREF, dependency on visual
information; SR-MANSOM, ability to manage distorted somatosensory inputs.

between PD-noFOG and controls. ABC (r ¼ 0.435, p ¼ 0.030) and FAB (r ¼ 0.451, p ¼ 0.024), while SR-
The multivariable model included all SR values as well as MANSOM was correlated with BBS (r ¼ 0.450, p ¼ 0.024). NFOGQ
UPDRS-III, BBS, ABC, BAI, and BDI scores (Table 2). Variables with a scores were also correlated with ABC (r ¼ 0.637, p ¼ 0.001), FAB
high risk of collinearity (SR-MANSOM: VIF ¼ 26.558 and SR-VEST: (r ¼ 0.471, p ¼ 0.017), and BBS (r ¼ 0.488, p ¼ 0.014) scores. SR-
VIF ¼ 12.846) were consecutively excluded. The remaining nine VISPREF remained correlated with NFOGQ (r ¼ 0.432, p ¼ 0.039)
variables in each regression model had VIFs < 5, indicating a low after controlling for ABC and FAB scores, while SR-MANSOM did not
risk of collinearity. The multivariable model including SR-VEST after controlling for BBS score (r ¼ 0.374, p ¼ 0.072).
identified SR-VEST as an independent risk factor for FOG among
PD patients. In the multivariable model including SR-MANSOM, SR- 4. Discussion
MANSOM was an independent risk factor for FOG and SR-VISPREF
tended to have an influence on FOG. Our study demonstrated that impaired processing of postural
sensory inputs was strongly related to the presence and severity of
3.3. Correlation analysis FOG in PD. Specific patterns of postural sensory deficits involving
recruitment of vestibular information and control over distorted
Spearman correlations revealed that NFOGQ scores correlated somatosensory inputs substantially contributed to FOG. Moreover,
with SR values for visual dependency (SR-VISPREF: r ¼ 0.660, correlation analysis revealed that PD-FOG with higher reliance on
p < 0.001) and the ability to control distorted somatosensory inputs visual information exhibited more profound freezing behavior. In
(SR-MANSOM: r ¼ 0.511, p ¼ 0.009) among PD-FOG addition, the severity of FOG was correlated with several clinical
(Supplemental Table 2). Also, SR-VISPREF was correlated with measures assessing FOF, global executive function, and clinical
balance performance.
The process of integrating sensory information to ensure
Table 2 postural control has been widely studied in PD patients using
Multivariable analysis of postural sensory contributors to FOG in PD patients.
quantitative posturography. These studies have mainly assessed the
SRs p ORa 95% CI relationship between postural sensory deficits and disease severity
Multivariable model including SR-VEST [16,18] or fall risk [10] and the effects of therapeutic interventions
SR-SOM 0.581 1.092 0.799e1.493 on postural control [17]. However, few studies systematically
SR-VIS 0.073 1.122 0.990e1.272 assessed postural sensory processing in PD patients with FOG [19],
SR-VEST 0.005 1.447 1.120e1.869 despite growing evidence from behavioral [4] and neuroimaging
SR-VISPREF 0.171 1.075 0.969e1.191
Multivariable model including SR-MANSOM
works [5,6] suggesting their potential relationship. Furthermore,
SR-SOM 0.504 1.116 0.809e1.538 although FOG and postural imbalance emerge from a disrupted
SR-VIS 0.138 0.775 0.553e1.085 interplay between motor, cognitive, and affective factors [1,20],
SR-VISPREF 0.056 0.695 0.478e1.009 these factors have been rarely considered in previous posturo-
SR-MANSOM 0.044 2.904 1.028e8.202
graphic studies. In addition, defining the unique patterns of
FOG, freezing of gait; PD, Parkinson's disease; SR, sensory ratio; OR, Odds ratio; CI, postural sensory loss in PD patients with FOG can promote the
confidence interval; SR-VEST, ability to use vestibular information; SR-SOM, ability efficacy of sensory cueing strategies for ameliorating FOG by more
to use somatosensory information; SR-VIS, ability to use visual information; SR-
VISPREF, dependency on visual information; SR-MANSOM, ability to manage dis-
accurately identifying suitable patients for these rehabilitative
torted somatosensory inputs. therapies. Our study gives some answers to these issues by delin-
a
Adjusted for UPDRS-III, BBS, ABC, BAI, and BDI scores. eating independent contributions of postural sensory deficits to
76 Y.E. Huh et al. / Parkinsonism and Related Disorders 25 (2016) 72e77
FOG in PD while also considering motor, cognitive, and affective
factors.
We found that the inability to integrate vestibular information
for postural balance was an important contributor to FOG. As none
of our PD patients showed sensory deficits involving peripheral
afferents, this finding may stem from a failure in the central pro-
cessing of vestibular feedback, consistent with previous studies
[16e18]. Several studies report abnormal central processing of
vestibular signals in PD. Altered vestibulocollic responses, which
represent neural circuits mediating postural balance, have been
documented in PD patients with moderate to severe motor
disability [21]. A previous posturographic study shows that PD
patients who experience falls exhibit impaired balance during the
SOT when postural control relies on vestibular information [22]. A
recent research reports improved balance control in PD patients
after applying galvanic stimulation activating the vestibular system
[23]. However, the relationship between vestibular dysfunction and
FOG is largely unknown in PD. Normally, vestibular feedbacks
become more important when initiating walking or turning [24],
when FOG is usually provoked in PD patients [1]. Direct projections
from vestibular nuclei to pedunculopontine nuclei, which are
involved in the generation of FOG [1,13], have been confirmed in
primates [25]. Recently, single cell recordings of pedunculopontine
nuclei in macaque monkeys reveal that vestibular stimuli enhance
the activity of these neurons [26]. Together with these previous
findings, our results indicate that impaired processing of vestibular
information to ensure balance plays an essential role in generating
FOG in PD.
In our PD-FOG, postural sensory processing was compromised
exclusively during distorted somatosensory conditions. This is in
line with a previous study demonstrating that somatosensory il-
lusions induced by tendon vibration impair force-matching re-
sponses during isometric contraction in PD patients with FOG [27],
suggesting deficits in processing distorted somatosensation. Our
results are further supported by the finding that a voluntary step
paradigm conjoined with somatosensory perturbation provokes
freezing-like knee trembling in PD patients with FOG [2], possibly
due to decoupling between anticipatory postural adjustments and
step motor programs. Therefore, postural sensory deficits involving
ineffective control over erroneous somatosensory information
could contribute to FOG, possibly by disrupting postural prepara-
tion process preceding steps.
Our correlation analysis revealed a relationship between visual
dependency and the severity of FOG among PD-FOG. PD patients
are known to rely heavily on visual information for locomotor
performance [8,28]. For instance, PD patients shows abnormally
increased postural sway in response to moving visual scene,
reflecting elevated visual dependency [28]. Similarly, our PD-FOG
swayed more during sway-referenced visual conditions, condi-
tions 3 and 6, and SR-VISPREF tended to predict the presence of
FOG. This result might be interpreted as a compensatory increment
of visual dependency to overcome more severe FOG, as visual cues
facilitate locomotion in PD by shunting a deficient internal trigger
of basal ganglia-supplementary motor area circuits [29]. Alterna-
tively, increased visual dependency could induce more severe
freezing behavior by entrapping PD-FOG to visual inputs, even if
unreliable, subsequently interrupting sensory processing [8]. Pro-
spective trials are needed to confirm a causal relationship between
visual dependency and FOG.
We found that several clinical parameters, including ABC, BBS,
and FAB scores, related to FOG and posturographic measures [1].
Given that postural sensory signals are utilized to generate refer-
ences for cognitive and limbic/affective processes during locomo-
tion, our data provide support for a recent model of FOG, which
proposes that FOG results from the paroxysmal overload of
dopaminergically-deficient striatal regions by complementary yet
competing motor-cognitive-limbic inputs (Supplemental
reference). Our PD-FOG showed lower ABC scores, reflecting
greater FOF. Moreover, PD-FOG with greater FOF showed more
severe FOG and higher reliance on visual information. These find-
ings are consistent with previous studies showing that FOF is
strongly associated with poorer gait and balance in PD [12], and is
also a main characteristic of several balance disorders, such as vi-
sual vertigo, that are often related to over-reliance on visual stimuli
[30]. In addition, we found that greater deterioration in executive
function was associated with more severe FOG and higher visual
dependency among PD-FOG. FOG is frequently related to executive
dysfunction, especially conflict resolution failure [3]. Accordingly,
poorer executive function can further delay selection of internal
locomotor representation, upon encountering environmental
changes, consequently compelling PD-FOG to rely more on
externally-driven visual stimuli [8] and eliciting more severe FOG.
Given this complex interaction between FOG and balance, cogni-
tive, and emotional factors, it is critical to incorporate these factors
into studies investigating FOG in PD [1].
Although impaired postural sensory processing is reported in
PD patients with moderate to severe motor disability [16,18],
postural sensory processing was generally preserved in our PD-
noFOG with similar disability. Instead, our PD-FOG showed
similar patterns of postural sensory impairment to those in previ-
ous posturographic studies [16,18]. Presumably, FOG may be, partly,
responsible for the impaired sensory processing observed in PD
patients in previous studies [16,18].
A couple limitations of our study should be noted. First, because
FOG is difficult to elicit in a laboratory setting, we could not exclude
the possibility that individuals classified as PD-noFOG might
experience FOG during daily activities. However, group classifica-
tion was based on both the NFOGQ and a turning-in-place task,
which reliably discriminate between PD patients with and without
FOG [11,14]. Thus, it is unlikely that individuals who had freezing
episodes would be included in PD-noFOG. Second, given the cross-
sectional design of this study, it remains uncertain whether
postural sensory deficits observed in our patients represent a pri-
mary pathology or a maladaptive change to compensate for pri-
mary damage. Longitudinal monitoring of postural sensory deficits
is needed to determine the nature of their relationship with FOG.
5. Conclusion
Our data demonstrate that specific patterns of postural sensory
deficits, including the inability to use vestibular inputs and poor
control over perturbed somatosensory feedbacks, contribute to
FOG in PD patients. Moreover, the severity of FOG is associated with
increased reliance on visual inputs. Quantitative assessment of
postural sensory deficits in PD patients with FOG may increase our
understanding of pathomechanisms of FOG and help identify pa-
tients who are suitable for employing sensory cueing strategies to
alleviate FOG. Future prospective studies investigating postural
sensory deficits in PD patients might lead to more quantitative
measures for identifying patients at a high risk of FOG and to the
development of rehabilitative therapies customized for PD patients
with specific sensory loss.
Authors roles
Young Eun Huh: Design of the study; acquisition of data;
analysis and interpretation of data; drafting the article and revising
it critically for important intellectual content; final approval of the
version to be submitted. Seonhong Hwang: Analysis of data,
revising the article critically for important intellectual content;
 Y.E. Huh et al. / Parkinsonism and Related Disorders 25 (2016) 72e77
final approval of the version to be submitted. Keehoon Kim:
Analysis of data, revising the article critically for important intel-
lectual content; final approval of the version to be submitted. Won-
Ho Chung: Conception and design of the study; acquisition of data;
revising the article critically for important intellectual content;
final approval of the version to be submitted. Jinyoung Youn:
Conception and design of the study; acquisition of data; revising
the article critically for important intellectual content; final
approval of the version to be submitted. Jin Whan Cho: Conception
and design of the study; acquisition of data; analysis and inter-
pretation of data; revising the article critically for important in-
tellectual content; final approval of the version to be submitted.
Conflict of interest
None.
Study funding
None.
Appendix A. Supplementary data
Supplementary data related to this article can be found at http://
dx.doi.org/10.1016/j.parkreldis.2016.02.004.
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