THE NATURE OF DUAL-TASK INTERFERENCE DURING GAIT

IN INCIDENT PARKINSONS DISEASE

L. ROCHESTER, * B. GALNA, S. LORD AND D. BURN
Institute for Ageing and Health, Newcastle University, Clinical
Ageing Research Unit, Campus for Ageing and Vitality,
United Kingdom
AbstractDual-task interference during gait is a common
phenomenon in older adults and people with Parkinsons
disease (PD). Dual-task performance is driven by cognitive
processes involving executive function, attention and work-
ing memory which underpin resource capacity and alloca-
tion. The underlying processes that contribute to dual-task
interference are poorly understood, and confounded by
methodological dierences. The aim of this study was to
explore the nature of dual-task interference in PD with
respect to age-matched controls. We examined 121 people
with early PD and 189 controls and controlled for baseline
task demand on both tasks allowing between-group dier-
ences to be attributed to dual-task interference rather than
dierences in baseline performance. We also compared a
wide range of gait characteristics to evaluate the pattern of
interference. Participants walked for two minutes at a pre-
ferred pace under single- and dual-task (test of working
memory capacity digit span recall) conditions. In a sub-
group task demand was increased (digit span +1) (n =55
control, n =44 PD) to assess the inuence of resource
capacity. Finally the association between dual-task interfer-
ence with motor and cognitive characteristics was examined
to evaluate resource capacity and allocation. PD and con-
trols responded similarly to the dual-task for all gait charac-
teristics except for step width and step width variability and
this was the same when task demand increased (dual +1).
Control participants took wider steps (p =0.006) and step
width variability increased signicantly for controls
(p =0.001) but not PD. Interference was specic to the gait
characteristic rather than a global pattern of impairment.
Digit span error rates were not signicantly dierent
between groups during dual-task performance. There were
no signicant correlations with dual-task interference and
global cognition, motor decit, and executive function for
either group. Eects of dual-tasks on gait performance are
twofold and specic to the gait characteristic. They reect
an age-related reduction in gait performance (especially
forward progression) in PD and controls possibly due to
reduced resource capacity; and secondly, show postural
stability during walking in early PD is disproportionately
aected highlighting a PD-specic dual-task co-ordination
decit. Further work is required to identify the cognitive,
executive and motor correlates of dual-task interference
from which inferences about underlying cognitive pro-
cesses can be made. These ndings inform an understand-
ing of dual-task impairment in early PD and suggest that
management should target postural control under dual-task
conditions fromthe early stages. 2014 IBRO. Published by
Elsevier Ltd. All rights reserved.
Key words: Parkinsons, gait, dual-task, postural control,
attention, step width variability.
INTRODUCTION
The ability to carry out two tasks at once is critical to
eective functioning in the real-world and decits
(termed dual-task interference) have been linked to loss
of independence and increased risk of falls (Beauchet
et al., 2009; Beurskens and Bock, 2012), although the
latter is controversial (Zijlstra et al., 2008; Beauchet
et al., 2009; Smulders et al., 2012). People with
Parkinsons disease (PD) describe diculties with dual-
task performance when walking (Jones et al., 2008) and
studies typically highlight a slower, more variable gait
when distracted by a dual-task (Hausdor et al., 2003;
Rochester et al., 2004; Yogev et al., 2005; Lord et al.,
2011; Kelly et al., 2012). Some evidence suggests
that people with PD are more aected by dual-tasks
than healthy older adults although this is by no means a
robust nding (Kelly et al., 2012). At present the
extent of dual-task interference in PD over and above
age-associated changes is unclear.
Dual-task gait interference in PD becomes evident
when attentional control cannot fully compensate for
motor impairment due to basal ganglia pathology. Dual-
task gait performance is supported by cognitive
processes such as executive function and attention
(Yogev-Seligmann et al., 2008) and theoretical models
such as the working memory system oer a framework
to understand the processes underlying dual-task
interference. The working memory system underpins the
ability to hold and manipulate information over brief time
periods and is limited by its capacity to process
information (resource capacity) and co-ordinate multiple
sources of information (resource allocation) (Baddeley,
http://dx.doi.org/10.1016/j.neuroscience.2014.01.041
0306-4522/ 2014 IBRO. Published by Elsevier Ltd. All rights reserved.
*
Corresponding author. Address: Institute for Ageing and Health,
Newcastle University, Clinical Ageing Research Unit, Campus for
Ageing and Vitality, Newcastle upon Tyne NE4 5PL, United Kingdom.
Tel: +44-(0)-191-248-1250; fax: +44-(0)-191-248-1251.
E-mail address: lynn.rochester@ncl.ac.uk (L. Rochester).
Abbreviations: ANCOVA, analysis of covariance; GDS, Geriatric
Depression Scale; MMSE, Mini Mental State Exam; OTS, One Touch
Stockings; PD, Parkinsons disease; PFC, prefrontal cortex; PIGD,
Postural Instability and Gait Disorder; PoA, Power of Attention; SD,
standard deviation; UPDRS, Unied Parkinsons Disease Rating Scale.
Neuroscience 265 (2014) 8394
83
1992). The working memory system draws on executive
functions to co-ordinate allocation of attention between
concurrent tasks and these are features associated with
the function of the pre frontal cortex (McCabe et al.,
2010). Both attention and executive function decits are
features of basal ganglia pathology even in early PD
(Williams-Gray et al., 2009), and both are associated
with dual-task interference (Amboni et al., 2013). Greater
attention to walking and/or cognitive impairments
(particularly executive function and attention) in PD may
therefore result in disproportionately greater interference
as a result of reduced resource capacity (working
memory capacity), resource allocation (dual-task co-
ordination decit within working memory) or, as some
authors have suggested, an inability to prioritize tasks
appropriately. However at present the nature of dual-
task interference in PD is unclear.
Certain features of gait have also been reported to be
more vulnerable to dual-task interference in PD. For
example swing time and swing time variability and
bilateral co-ordination of lower limb movements are
especially sensitive (Yogev et al., 2005; Plotnik et al.,
2009). Whether dierent gait characteristics are
selectively vulnerable to dual-task interference however
is not clear due to inconsistent reporting and a broader
understanding may help explain the association of dual-
task impairment with fall risk. The question therefore
remains as to the extent of dual-task interference in PD
with respect to individual gait characteristics.
Methodological issues often confound interpretation,
for example: controlling for baseline task demand such
that dual-task performance cannot be attributed to
dierences in single-task performance between groups;
reporting performance on both tasks to assess combined
dual-task decit to account for trade-o (task
prioritization) in performance between tasks; and dierent
methods of calculating dual-task decits (Dalrymple-
Alford et al., 1994; Cocchini et al., 2004; Logie et al.,
2004; Foley et al., 2013; Fuller et al., 2013). Studies of
dual-task interference in PD do not consistently address
these methodological criticisms which most likely explain
the inconsistent ndings. Further they are typically
carried out in more advanced cohorts and a better
understanding of the early features of dual-task
interference is important to fully understand fall risk and
develop appropriate and timely therapeutic intervention.
We aimed to characterize dual-task performance
during gait in people with early PD with respect to age-
matched controls to: quantify the extent of dual-task
interference; shed light on the nature of the underlying
dual-task decit; and compare the vulnerability of
dierent features of gait to dual-task interference. From
our work and others we used a protocol adapted for gait
which was informed by a theoretical model of working
memory (Baddeley, 1992; Cocchini et al., 2004; Hamilton
et al., 2009) which allowed us to more fully explore the
cognitive processes (resource capacity and allocation)
underpinning interference. The protocol also directly
addressed previous methodological concerns. Our
primary hypothesis was that dual-task interference would
be disproportionately greater in PD compared to age-
matched controls as a consequence of resource
capacity, resource allocation or task prioritization decits.
We also hypothesized that dual-task interference would
be greater in gait characteristics that are more directly
inuenced by cognition (e.g. mean walking speed, step
length and step time).
EXPERIMENTAL PROCEDURES
Participants
People with PD were recruited within 4 months of
diagnosis of idiopathic PD as part of an incident cohort
study of people with PD (Khoo et al., 2013). Participants
were excluded if they had any neurological (other than
PD), orthopedic or cardiothoracic conditions that may
have markedly aected their walking or safety during
the testing sessions. In addition, PD participants had to
be diagnosed with idiopathic PD according to the UK
Parkinsons Disease Brain Bank criteria by a movement
disorders specialist (Gibb and Lees, 1988), and were
excluded if they presented with signicant memory
impairment (Mini Mental State Exam (MMSE) 6 24)
(Folstein et al., 1975), dementia with Lewy bodies,
drug-induced parkinsonism, vascular parkinsonism,
progressive supranuclear palsy, multiple system
atrophy, cortico-basal degeneration or poor command of
English. Control participants were recruited from
research-active general practices via a regional primary
care research network, from local hospital trusts via
advertising, and via the Public Engagement Team
based at Newcastle University. Inclusion criteria were:
(1) greater than 60 years of age; (2) able to walk
independently without a walking aid; and (3) no
signicant cognitive impairment, mood or movement
disorder. This study was conducted according to the
declaration of Helsinki and had ethical approval from the
Newcastle and North Tyneside research ethics
committee. All participants signed an informed consent
form prior to testing.
Demographic and clinical measures
Age, sex and body mass index (BMI) were recorded for
each participant. The severity of PD motor symptoms in
the PD participants was measured using the Hoehn and
Yahr scale (Hoehn and Yahr, 1967) and section III of the
modied Movement Disorder Society version of the
Unied Parkinsons Disease Rating Scale (UPDRS III)
(Goetz et al., 2007). The Postural Instability and Gait
Disorder (PIGD) and Tremor subscales (nine and ve
items respectively from the new-UPDRS III scale) were
also calculated from the New UPDRS (Goetz et al.,
2007) to examine the impact of motor capacity on dual-
task interference. The scales were used as continuous
variables for correlational analysis. Balance self-ecacy
was measured using the Activities Balance Self
Condence Scale (Powell and Myers, 1995). Depression
was measured with the Geriatric Depression Scale
(GDS) (Schrag et al., 2007). Levodopa equivalent dose
(LEDD) scores were calculated according to established
84 L. Rochester et al. / Neuroscience 265 (2014) 8394
methods (Tomlinson et al., 2010). In addition, executive
function was measured using Power of Attention (PoA)
(Wesnes, 2002) and mean latency to correct response
on the One Touch Stockings (OTS) of Cambridge from
the computerized Cambridge Neuropsychological Test
Automated Battery (CANTAB) (Robbins et al., 1994).
Walking protocol
Gait was assessed using a 7-m-long 0.6-m-wide
instrumented walkway (Platinum model Gaitrite, software
version 4.5, CIR systems, United States of America)
under (i) single-task and (ii) dual-task walking conditions.
The Gaitrite mat is a valid and reliable method for
measuring gait characteristics in older adults with and
without pathology (Menz et al., 2004; Galna et al., 2013).
Participants were instructed to walk at their comfortable
walking pace for two minutes around a 25-m oval
circuit. Their gait was repeatedly sampled as they
walked over the Gaitrite mat which was placed in the
circuit as reported elsewhere (Galna et al., 2013). The
order of single-task and dual-task walking conditions was
randomized across participants. PD participants were
tested approximately 1 hour after medication intake.
Gait outcomes
Gait outcomes were selected from a model of gait we
developed for older adults (Lord et al., 2013a) and
validated in PD (Lord et al., 2013b) that comprises 16
gait variables describing ve independent domains of
gait. Selection was based on our a priori understanding
of primary PD-specic gait pathology, secondary change
in gait arising from compensation and characteristics
that best discriminate early PD and controls. The
domains and selected outcomes were: (1) Pace domain:
step velocity (m s
1
) and step length (m); (2) Variability
domain: standard deviation (SD) of step length and step
time; (3) Rhythm domain: step time (ms); (4) Postural
control domain: step width variability (SD) and step
width (m); (5) Asymmetry domain: step length and
stance time asymmetry (ms). Full details of the testing
procedure for gait and derivation of outcomes are
described elsewhere (Lord et al., 2013a). Briey, the
mean and variance of left steps and right steps were
calculated separately. Mean gait characteristics were
then calculated as the mean of left and right step
means, gait variability characteristics were calculated as
the square root of the mean variance of left and right
steps (resulting in the combined standard deviation of
left and right steps independent of gait asymmetry), and
gait asymmetry was calculated as the absolute
dierence between left and right step means.
In this study the eect of the dual-task on gait
performance was described as dual-task interference
and calculated as the raw dierence between dual-task
and single-task performance (Eq. (1)):
Dual-task interference Dual-task performance
Single-task performance 1
Dual-task interference is also commonly expressed as
proportional to single-task performance, we therefore present
percentage of dual-task interference in Fig. 1, as calculated in
Eq. (2):
Percentage of dual-task interference

Dual-task performance Single-task performance

Single-task performance
2
Cognitive protocol
The Wechsler Forward Digit Span was used as the
concurrent cognitive task (Wechsler, 1997) because it is
a validated test of working memory and has been used
in our previous dual-task research (Logie et al., 2004;
Hamilton et al., 2009). This test can be adjusted to
match individual performance levels and manipulated in
a controlled way to reduce the capacity of working
memory in order to observe eects on interference. The
test also aimed to minimize structural interference. Each
participant was tested at their maximum forward digit
span which was determined in sitting and dened as the
longest digit span the participant could successfully
recall in two out of three attempts. Strings of digits
consisted of pre-recorded numbers presented at a
frequency of 1/s through a speaker system (Creative,
Inspire S2, Singapore). Participants were tested at their
maximum digit span to allow baseline performance and
therefore task demand to be controlled according to the
ability of each participant. Any between-group
dierences for dual-task performance were therefore not
simply due to dierences in capacity for single-task
performance (Logie et al., 2004).
Prior to walking conditions, participants recalled
strings of digits (at their maximum digit span) for two
minutes while sitting. For the dual-task conditions,
participants listened to strings of digits while walking
and repeated them back. A subset of participants also
completed the task at an increased level by adding an
additional digit to the participants maximum digit span
(termed the dual + 1 condition) in order to increase
demand on working memory. During both dual-task
-25% -15% -5% 5% 15% 25%
Step velocity
Step length
Step me
Step length variability
Step me variability
Stance me asymmetry
Step length asymmetry
Step width
Step width variability
Digit span recall
Control
PD
*
Dual-task interference
(dual task - single task) single task
*
Fig. 1. Percentage of dual-task interference for control (n = 184)
and PD (n = 121) participants.

Signicant interaction in dual-task
interference between groups (p < 0.05).
L. Rochester et al. / Neuroscience 265 (2014) 8394 85
conditions participants were instructed to concentrate on
both the digits and your walking. Error rate on the digit
span task was calculated for each condition as the
number of strings incorrectly recalled divided by the total
number of strings attempted.
Data analysis and statistics
Data analysis was carried out using SPSS v19 (IBM).
Independent t-tests and MannWhitney U tests were
used to compare control and PD participants for clinical,
cognitive and demographic variables. Gait performance
was compared under single- and dual-task conditions
using an analysis of variance (ANOVA) with groups as a
between-subject factor, controlling for age and sex. Chi-
squared tests were used to test group dierences in
maximum forward digit span.
To test our primary hypothesis that dual-task
interference would be greater in PD we compared dual-
task interference in PD and control participants using an
analysis of covariance (ANCOVA) with group (PD,
control) as a between-subject factor and task condition
(single, dual) as a repeated measures factor, with main
eects and interactions for group and task condition.
The same model of ANCOVA was used to test the
eect of dual-task interference on digit recall. We then
addressed specic sub-questions to explore the nature
of dual-task interference with respect to resource
capacity, task prioritization, and resource allocation as
follows:
1. The eect of resource capacity was tested by
increasing demand on working memory (dual + 1
condition) in a subset of PD participants using
the same statistical approach as described above
and the dual-task repeated measures factor
included the two levels (Single, Dual + 1) for the
ANCOVA. Age, sex and order of dual-task presen-
tation were entered as covariates. The same
model of ANCOVA was used to test the eect of
dual-task interference on digit recall.
2. Resource capacity and resource allocation were
also explored by examining the relationship
between motor (UPDRS III, PIGD subscore) and
cognitive impairment (MMSE, OTS, PoA) on
dual-task interference using partial correlations,
controlling for order of dual-task presentation.
3. Task prioritization (trade-o) of performance
between gait and digit span under dual-task condi-
tions was assessed using partial correlations
between dual-task interference for each gait char-
acteristic with the error rate during the digit span
test, controlling for order of dual-task presentation.
We tested a range of gait outcomes allowing us to
compare the extent of interference on each outcome
addressing our secondary hypothesis. All non-normal
distributions of continuous variables were transformed
before parametric tests. A p value of <0.05 was used
to guide interpretation of statistical signicance of
ANCOVA after Bonferroni correction for multiple post
hoc comparisons. A more conservative p < 0.01 was
chosen for bivariate correlations to accommodate
multiple tests.
RESULTS
Participant demographic, clinical and cognitive
descriptors are shown in Table 1. Compared to controls,
the PD participants were younger (mean dierence
2.5 years), included proportionally less women (controls:
58%; PD 33%), had less balance condence; poorer
cognition; and increased fatigue. Although depression
scores were greater in PD participants this remained
within the normal range. People with PD were in the
early stages of the disease with mild to moderate motor
symptoms. Gait performance for all variables except
step width and step length asymmetry was impaired in
PD compared to controls for single-task gait. There was
no dierence in maximum forward digit span between
groups or number of errors made on the digit span
recall for single-task (i.e. in sitting).
Eect of dual-tasks on gait and cognitive
performance
Dual-task gait interference and statistical comparisons for
each group are summarized in Table 2 and 3. Dual-task
interference (main eects) was observed for four of the
nine gait variables (step velocity, step length, step time
and step length asymmetry) with signicantly decreased
dual-task gait performance, however this was the same
for both PD and controls. There was no signicant
change for step length variability, step time variability
and stance time asymmetry during the dual-task for
either group. There was a signicant group * task
interaction for step width (p = 0.006) and step width
variability (p = 0.002) (Fig. 1). Although both control
(p < 0.001) and PD (p < 0.001) participants took wider
steps under dual-task conditions, this was greater for
control participants compared to PD participants
(p = 0.006). Step width variability did not change
signicantly in PD during the dual-task compared to
controls who showed a signicant increase (p = 0.001).
There was no signicant change in the error rate for the
digit span during dual-task performance for both PD and
controls.
Eect of increased dual-task demand
In a subset of 55 controls and 44 PD participants we
increased dual-task demand (dual + 1 condition)
which increased gait interference to a similar extent in
PD and control groups. Main eects were shown for
seven out of nine variables (step velocity, step length,
step time, variability of step time and step length, step
length asymmetry, step width) (no group dual-task
interactions) (Table 3). There was a signicant
interaction eect for step width (p = 0.014), whereby
control participants widened their step width under
dual + 1 conditions (p = 0.001) yet PD participants did
not (p = 0.423). Digit span errors signicantly increased
under the dual + 1 conditions however this was the
same for PD and control groups (no interactions).
86 L. Rochester et al. / Neuroscience 265 (2014) 8394
Relationship of motor and cognitive features with
dual-task interference
There were no signicant correlations of any motor or
cognitive variables with dual-task gait interference or
error rate on the digit span for either group (Table 4).
Relationship between gait performance and digit
span errors
Changes in task prioritization (trade-o) between tasks
were evaluated by testing the relationship between dual-
task gait interference and error rate on the digit span
and there were no signicant correlations. Further
examination of individual responses under dual-task
conditions with respect to both gait performance and
errors on the digit span task showed that individual
strategies were highly inconsistent for both PD and
controls for all gait variables (Fig. 2 shows step velocity,
step width and step width variability). The results
therefore show no consistent prioritization of task for
either group.
DISCUSSION
The specic aim of this study was to characterize the
eect of dual-tasks on gait performance in PD and
explore the underlying nature of the decit. To this end,
we have conducted the largest investigation of dual-task
performance on gait in PD with controls to date. The
key nding from this study was that dual-task
interference during gait was comparable for early PD
and controls which suggest an age-related reduction in
resource capacity. Gait characteristics that reect
postural stability show a disproportionate eect
suggesting a dual-task co-ordination decit in PD. The
threshold for dual-task gait interference is also selective
to the gait characteristic with those under conscious
control showing the lowest threshold and greatest
interference.
Resource capacity contributes to dual-task decits in
PD and older adults
We hypothesized that dual-task impairment would be
disproportionally greater in PD compared to age-
matched controls. Contrary to our hypothesis and
previous research (e.g. Hausdor et al., 2003;
Rochester et al., 2004) we found that dual-task
interference was similar for PD and control participants
for most gait characteristics, even with increased task
demand (dual + 1). Error rates on the digit span task
were not signicantly dierent during the dual-task for
Table 1. Clinical and demographic characteristics of PD and control participants, and performance on single-task gait and digit recall tasks. Group
means have been adjusted for age and sex dierences between groups for single-task performance.
Characteristic Controls (n = 184)
Mean (SD)
PD (n = 121)
Mean (SD)
p
Male/female (n)
*
m 78, f 106 m 81, f 40 <0.001
Age (years) 69.4 (7.7) 67.0 (10.4) 0.024
MMSE (030) 29.2 (1.0) 28.6 (1.3) <0.001
MoCA (030)

27.1 (2.4) 25.1 (3.5) <0.001

GDS (015) 1.1 (1.8) 2.6 (2.1) <0.001
Power of Attention (ms) 1303 (156) 1357 (201) 0.010
One Touch Stockings (mean latency to correct response, s) 17.9 (11.7) 22.4 (15.2) 0.009
MFI physical fatigue (020) 8.2 (3.6) 10.5 (4.2) <0.001
ABCs (0100%) 91.8 (10.9) 82.5 (18.9) <0.001
Sit to stand (s) 12.4 (3.9) 13.7 (4.3) 0.018
Hoehn and Yahr stage (n) HY I 28, HY II 72, HY III 21
Levodopa equivalent daily dose (mg) 176.2 (143.1)
MDS-UPDRS III 25.5 (10.4)
PIGD subscore 0.626 (0.385)
Single-task performance
Step velocity (m s
1
) 1.27 (0.19) 1.10 (0.21) <0.001
Step length (m) 0.68 (0.08) 0.61 (0.10) <0.001
Step time (ms) 540 (48) 556 (48) 0.006
Step length variability (m) 0.020 (0.006) 0.023 (0.008) <0.001
Step time variability (ms)

2.73 (0.30) 2.91 (0.34) <0.001

Stance time asymmetry (ms)

2.70 (1.34) 3.61 (1.92) <0.001

Step length asymmetry (m)

0.13 (0.06) 0.14 (0.07) 0.083

Step width (m) 0.091 (0.025) 0.090 (0.030) 0.826
Step width variability (m) 0.022 (0.005) 0.019 (0.006) <0.001
Digit span (median, range)
*
6 (4, 9) 6 (4, 8) 0.104
Error rate on digit span (%) 24.1 (21.7) 25.9 (20.1) 0.520
MMSE: Mini Mental State Exam; MoCA: Montreal Cognitive Assessment; GDS: Geriatric Depression Scale; MFI: Multidimensional Fatigue Inventory; ABCs: Activities-
specic Balance Condence scale; MDS-UPDRS III: Movement Disorders Society version of the Unied Parkinsons Disease Rating Scale (motor section); PIGD: Postural
Instability and Gait Disorder.
*
Chi-squared analysis.

Data for 115 PD participants and 89 controls.

Step time variability log transformed and asymmetry variables square root transformed.
L. Rochester et al. / Neuroscience 265 (2014) 8394 87
either group, suggesting that cognitive process during
dual-task testing were comparable. During the dual + 1
condition, both PD and control participants made more
errors on the digit recall task, indicating that the
cognitive load of this more dicult condition impacted
on working memory to a greater extent. Our results
therefore show that our protocol achieved a level of
diculty to cause dual-task interference ruling this out
as a potential explanation for the dierences. The most
likely explanation for our ndings is methodological. We
controlled for dierences in baseline performance by
standardizing task demand according to individual ability
on both tasks. Our intention was to avoid the
overestimation of dual-task interference that occurs as a
result of between-group dierences in baseline
performance (and its inuence on working memory
capacity), a feature observed in previous studies (Logie
et al., 2004). For example, Cocchini et al., found that
gait performance in Alzheimers disease was
disproportionately aected during dual-task performance
compared to controls, however, when they controlled for
baseline performance of the concurrent cognitive task
dual-task gait interference remained although
dierences between AD and older adults disappeared
Table 2. Gait and digit span performance during dual-task conditions. Values are shown as Mean SD
Variable Dual-task
Control PD
n = 184 n = 121
Dual-task gait performance
Step velocity (m s
1
) 1.20 0.20 1.04 0.22
Step length (m) 0.66 0.08 0.58 0.10
Step time (ms) 552 55 568 54
Step length variability (m) 0.022 0.006 0.025 0.009
Step time variability (ms)
*
2.89 0.35 3.07 0.36
Stance time asymmetry (ms)
*
2.86 1.52 3.91 1.99
Step length asymmetry (ms)
*
0.134 0.060 0.148 0.076
Step width (m) 0.096 0.027 0.093 0.031
Step width variability (m) 0.024 0.006 0.018 0.005
Error rate on digit span (%) 18.8 20.0 21.9 17.6
Dual-task interference (dual-task single-task performance, see Eq (1))
Step velocity (m s
1
) 0.069 0.086 0.068 0.067
Step length (m) 0.025 0.026 0.027 0.027
Step time (ms) 12.2 23.9 12.3 11.6
Step length variability (m) 0.0025 0.0059 0.0018 0.0021
Step time variability (ms)
*
3.28 7.32 3.53 3.44
Stance time asymmetry (ms)
*
1.42 9.19 2.55 2.58
Step length asymmetry (m)
*
0.0008 0.009 0.0016 0.0016
Step width (m) 0.0051 0.0081 0.0022 0.0023
Step width variability (m) 0.0012 0.0049 0.0007 0.0007
Error rate on digit span (%) 5.4 18.3 4.1 19.5
Group means have been adjusted for age, sex and order of dual-task presentation.
*
Step time variability log transformed and asymmetry variables square root transformed for dual-task performance. Untransformed data was
used to calculate dual task interference.
Table 3. Results of the ANCOVA to test for dual-task main eects and dual task interactions for the whole cohort and the subgroup who performed
the dual-task + 1 condition, adjusting for age, sex and order of dual-task presentation. F (p)
Variable Dual-task main eect Group Dual-task interactions
Single versus
dual-task
Single versus dual-
task + 1
Control versus PD (single and
dual-task)
Control versus PD (single and
dual-task + 1)
Step velocity (m s
1
) 26.4 (<0.001) 40.3 (<0.001) 0.094 (0.759) 0.746 (0.390)
Step length (m) 58.8 (<0.001) 52.8 (<0.001) 1.25 (0.264) 1.04 (0.312)
Step time (ms) 14.1 (<0.001) 18.1 (<0.001) 0.087 (0.769) 0.005 (0.942)
Step length variability (m) 2.60 (0.108) 17.0 (<0.001) 0.433 (0.511) 0.425 (0.516)
Step time variability (ms) 2.76 (0.098) 17.8 (<0.001) 0.021 (0.886) 0.017 (0.896)
Stance time asymmetry
(ms)
1.22 (0.271) 1.16 (0.284) 0.747 (0.388) 0.427 (0.515)
Step length asymmetry (m) 6.15 (0.014) 5.15 (0.025) 0.003 (0.957) 0.001 (0.983)
Step width (m) 2.43 (0.120) 6.67 (0.011) 7.61 (0.006) 7.55 (0.007)
Step width variability (m) 2.34 (0.127) 1.07 (0.304) 9.91 (0.002) 1.59 (0.210)
Error rate on digit span (%
incorrect)
0.731 (0.393) 15.5 (<0.001) 0.348 (0.556) 2.12 (0.149)
Values in bold and italics font indicate statistically signicant ndings (p < 0.05).
88 L. Rochester et al. / Neuroscience 265 (2014) 8394
(Cocchini et al., 2004). The authors concluded that the
dual-task interference was due to increased reliance on
executive function with aging to compensate for age-
related reductions in physical capacity which reduces
available resource capacity. In practical terms these
results have greater implications for functional
independence because motor function is already
compromised. Increased cognitive activity associated
with aging is evident in functional brain imaging studies
and thought to be related to increased sensory
processing (Heuninckx et al., 2005) and greater reliance
on controlled/cognitive processing over automatic
processing. Imaging studies of gait and postural control
also show dierent cognitive activity with aging, with
increased multisensory cortical and frontal control
indicating a more conscious strategy (Zwergal et al.,
2010). Together these features reduce automatic
processing and may place greater demands on resource
capacity potentially explaining dual-task interference.
Dual-tasks cause a disproportionate eect on
postural control in PD
The only dierence in dual-task interference between PD
and controls was for step width and step width variability,
both of which reect postural control in the mediolateral
direction (Gabell and Nayak, 1984; Brach et al., 2005,
2008) lending some support to our primary hypothesis.
Biomechanical models of gait show walking is inherently
unstable in the mediolateral direction, requiring active
control through a closed feedback loop to maintain
balance (Bauby and Kuo, 2000; Wuehr et al., 2013).
When there is an increased threat to stability (such as
dual-task performance) we would expect step width
variability to increase for greater adaptation and step
width to increase to compensate for potential instability
(Bauby and Kuo, 2000), and indeed that is what we saw
in the control participants. PD participants were however
unable to modulate step width variability suggesting a
greater risk to postural stability when engaged in more
complex tasks. While people with PD did increase their
step width under dual-task conditions this was less
eective than controls despite there being no baseline
dierences between groups in this characteristic. Others
have also reported selective eects of dual-tasks on
bilateral co-ordination during gait (Plotnik et al., 2009).
Why gait characteristics representative of postural
control are especially vulnerable to dual-task
performance in PD is unclear. Yogev-Seligmann and
colleagues found age-related dierences in DT
performance and argue that walking represents a
complex motor task requiring bilateral co-ordination and
dynamic postural control, both of which are monitored
by cognitive processes (Yogev-Seligmann et al., 2013).
Disturbance in postural control is a very early feature of
PD (Mancini et al., 2009; Schoneburg et al., 2013) and
disturbed sensory integration of proprioceptive
information is thought to be an important contributory
mechanism (Carpenter and Bloem, 2011; Schoneburg
et al., 2013). Sensory impairments are also found to
contribute to step width and step width variability in
older adults (Brach et al., 2008). In addition cognition is T
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L. Rochester et al. / Neuroscience 265 (2014) 8394 89
recognized to contribute to postural control (Boisgontier
et al., 2013). Together these features will increase
cognitive control of balance while walking potentially
reducing resource capacity and allocation and
increasing susceptibility to dual-task interference. The
results therefore suggest a dual-task co-ordination
decit specic to postural control which is a distinct
pathological eect of PD over and above aging, the
nature of which is explored further below.
The nature of dual-task interference: Resource
capacity or resource allocation?
To further explore the impact of resource capacity and
resource allocation on dual-task performance we
examined the association between motor and cognitive
variables, and interference. We expected that motor
capacity (measured by UPDRS III and PIGD subscore),
cognitive capacity (MMSE score) and resource allocation
(attention, OTS) would be associated with dual-task
interference, but were surprised to nd this was not the
case despite being signicantly dierent from controls. A
possible explanation includes the relatively mildly
aected PD group. Reported associations between
reduced executive function, attention and increased
dual-task interference in PD were found in more
advanced PD where the magnitude of dual-task
interference was also much greater (Rochester et al.,
2008; Lord et al., 2010). Stronger associations are likely
to emerge with disease progression and this is the focus
of an on-going longitudinal study.
The nature of dual-task interference: A problem with
task prioritization?
Error rates on the digit span task were not signicantly
dierent during the dual-task for either group,
suggesting a similar approach to allocation of cognitive
resource. Instructions were given to divide attention
between tasks therefore the net eect was an overall
decrease in performance when considering both gait
and cognitive responses and therefore no trade-o
eect (or task-prioritization strategy) between tasks. In
fact individual responses under dual-task conditions
were highly variable in agreement with others (Smulders
et al., 2012) a nding supported by the lack of
association between gait and digit span errors. This
suggests there is no denitive strategy regarding task
prioritization in contrast to earlier assertions (Bloem
et al., 2006). A recent study in 263 people with mild to
-0.4
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Digit span errors (Dual - Single) (% of errors/trial)
Control
PD
A
-0.04
-0.02
0
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0.04
-100% -50% 0% 50% 100%
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Digit span errors (Dual - Single) (% of errors/trial)
B
-0.02
-0.01
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-100% -50% 0% 50% 100%
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Digit span errors (Dual - Single) (% of errors/trial)
C
Fig. 2. Scatterplot comparing dual-task interference on gait and cognitive tasks. Dual-task interference is shown for step velocity (Panel A), step
width (Panel B) and step width variability (Panel C) and compared to dual-task interference for digit span recall in controls (open squares) and PD
participants (lled diamonds).
90 L. Rochester et al. / Neuroscience 265 (2014) 8394
moderate PD cited wide variation in response as the
reason why dual-task impairment did not predict falls
(Smulders et al., 2012). The mediators of dual-task
interference are varied and complex, and include motor
and cognitive function, cognitive reserve and
compensatory abilities, personality, aect and expertise
(Yogev-Seligmann et al., 2012). It is therefore clear that
simply considering the group eect of dual-task
performance provides a limited picture and individual
responses are important when interpreting ndings in
the clinic.
Dual-task inuences gait characteristics in a specic
rather than global manner
In both PD and older adults signicant dual-task
interference in velocity, step length, step time (forward
progression) and step length asymmetry was observed.
However, there were also some notable exceptions for
example, step time and step length variability which are
consistently reported as susceptible to dual-task
performance in PD and older adults (Hausdor, 2007).
The dual + 1 task caused a more global dual-task gait
interference in both groups with seven out of nine
variables showing signicantly reduced performance
compared to single task (no interactions). Our ndings
that dual-task interference increases with increased task
diculty concur with others (Rochester et al., 2004;
Yogev et al., 2005). In addition, the threshold for dual-
task interference is dierent depending upon the gait
characteristic (Yogev et al., 2005; Holtzer et al., 2012).
This raises the question of why specic gait
characteristics are more sensitive to task demand. A
potential explanation may be that cognition penetrates
those variables under conscious control (such as gait
speed, step length, cadence and step width) at a lower
threshold than those that occur on a millisecond basis
and are less amenable to online control (such as
variation in the step-to-step uctuations of gait). Our
ndings are also in line with our secondary hypothesis
that dual-task interference would be greater in those
characteristics under conscious control. The extent to
which these ndings represent a conscious strategy to
increase safety or a pathological instability in locomotor
control is unclear.
Neural correlates of dual-task gait interference
The locus of dual-task control is unclear and therefore the
precise mechanism contributing to interference
particularly with respect to a dual-task co-ordination
function is not certain (Boisgontier et al., 2013). In
general, evidence from imaging studies suggests a
distributed cognitive network with diverse cortical activity
on fMRI which increases under dual-task conditions
(Burgess et al., 2000; Boisgontier et al., 2013). Cortical
activity is also increased under dual-task conditions in
PD, for brain regions including the cerebellum, premotor
area, parietal cortex, precuneus and prefrontal cortex
(PFC) (Wu and Hallett, 2008). Understanding dual-task
interference in gait is more complex as it is dicult to
capture in imaging studies. Studies utilizing functional
near-infrared spectroscopy (fNIRS) allow dual-task
interference to be studied while subjects are walking,
however the data are conicting. Evidence suggests
activity in the PFC (an area involved in higher order
cognitive functions, namely executive function) is
increased under dual-task walking conditions, however
this is less ecient in older adults which may suggest
they under-utilize these cognitive functions (Holtzer
et al., 2011). Others have reported that activity in the
PFC is greater in older versus young adults (Ohsugi
et al., 2013). It is however uncertain as to the precise
mechanism underpinning dual-task gait interference at
present.
With respect to the concurrent tasks in our study we
selected a digit span as our cognitive task to minimize
structural interference during dual-task testing which
draw on frontal lobe functioning (McCabe et al., 2010).
It is possible that some overlap occurred given that
some aspects of cognitive function are also common to
gait, particularly activity in the PFC and this may have
contributed to the interference observed.
Study strengths
Strengths of this study include the large incident PD
cohort identied through a robust process (Khoo et al.,
2013) and are therefore representative allowing
generalizability of our study ndings. Furthermore we
included a control cohort allowing us to compare the
inuence of dual-task interference with respect to age,
sex and pathology, a feature that has received less
attention in the literature. We controlled for task demand
on both tasks by using self-selected task performance
which avoids the potential for confounding in previous
reports and allowed true dual-task interference to be
determined. This method has been advocated by others
to selectively identify pathology-specic impairments
(Logie et al., 2004; Hamilton et al., 2009). We also
report changes in performance on both gait and the
cognitive task. This allowed results to be interpreted in
relation to motor and cognitive capacity as well as task
prioritization allowing the nature of dual-task
interference in PD to be explored in detail. On the basis
of our ndings we recommend that baseline
performance is controlled for in order to avoid
overestimation of dual-task interference. We report a
wide range of gait characteristics which show selective
vulnerability to dual-task performance and task demand.
These ndings have important implications for
assessment with a broad gait assessment
recommended to understand the specic relationship of
gait interference and its implications; and management
of dual-task decits such as an early focus on training
postural control under dual-task conditions.
Study limitations
There are some study limitations that require comment.
We did not use dierent dual-tasks and therefore cannot
comment on whether the eect we see is restricted to
this type of task. In order to derive clear interpretations
of data it is necessary to be clear regarding structural
L. Rochester et al. / Neuroscience 265 (2014) 8394 91
interference. Although we aimed to deliver two tasks that
had minimal structural interference, it is very dicult when
evaluating complex skills such as gait due to the
widespread neural involvement (Nutt et al., 2011). In
addition, it is possible that more specic PD decits may
have been seen if exposed to a more complex
environment with unpredictable distractions or if we
tested people with more severe PD. On a practical level,
the functional impact of dual-task impairment in PD is
likely to be greater as their baseline gait performance is
more impaired.
CONCLUSIONS
Dual-task interference in PD is complex and inuences
gait in two distinct patterns: an age-associated reduction
in gait performance unrelated to pathology; and a PD-
specic eect showing a dual-task co-ordination decit
which aected postural control suggesting reduced
stability and ability to adapt under dual-task conditions.
The threshold for dual-task gait interference diers
depending upon the characteristic with those under
conscious control showing the lowest threshold and
greatest interference. Resource capacity (working
memory) accounts for these ndings while the role of
resource allocation is currently unclear. Further work is
required to identify the cognitive, executive and motor
correlates of dual-task interference from which
inferences about the contributing cognitive processes
can be made and longitudinal studies are needed to
explore evolution of interference over time. The ndings
point to the need to control for baseline dierences to
avoid overestimating dual-task impairment and to
instigate training to reduce dual-task related changes in
postural control during gait from the early phase of PD.
FINANCIAL DISCLOSURES
L.R. research program is supported in part by grants from
the Medical Research Council, European Union
Framework 7, Parkinsons UK, the Michael J Fox
Foundation, the National Institute for Health Research
Biomedical Research Unit for Lewy Body Dementias
(NIHR BRU) and NIHR HTA and GlaxoSmithKline and
has received honorarium for lecture from
GlaxoSmithKline. D.B. is supported by grants from
Parkinsons UK, NIHR and Welcome Trust and has
received consultancy from Michael J Fox Foundation
and honorarium for lectures from Teva-Lundbeck and
UCB. B.G. and S.L. have nothing to declare.
AUTHOR CONTRIBUTION
L.R.: Study concept and design, interpretation of data,
drafting and critical revision of manuscript for important
intellectual content.
B.G.: Acquisition of data, statistical analysis and
interpretation.
S.L.: Study design, acquisition of data, interpretation
of data, critical revision of manuscript for important
intellectual content.
D.B.: Critical revision of the manuscript for important
intellectual content.
AcknowledgmentsThe research was supported by the National
Institute for Health Research (NIHR) Newcastle Biomedical Re-
search Unit based at Newcastle upon Tyne Hospitals NHS Foun-
dation Trust and Newcastle University. The research was also
supported by NIHR Newcastle CRF Infrastructure funding. The
views expressed are those of the authors and not necessarily
those of the NHS, the NIHR or the Department of Health. We
would like to acknowledge Mrs. Dadirayi Mhiripiri for her assis-
tance with data collection.
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(Accepted 21 January 2014)
(Available online 4 February 2014)
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