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Compensation Strategies for Gait Impairments
in Parkinson Disease
A Review
Jorik Nonnekes, MD, PhD; EvženRůžička, MD, DSc; Alice Nieuwboer, PhD; Mark Hallett, MD;
Alfonso Fasano, MD, PhD; Bastiaan R. Bloem, MD, PhD
Gait disorders in Parkinson disease (PD) are among the most
disabling symptoms of the disease because they signifi-
cantly limit mobility and often result in falls and fall-
associated injuries. Gait impairments in PD range from a reduced gait
speed and smaller stride length to freezing of gait (FOG), which is
characterized by sudden, relatively brief episodes of inability to pro-
duce effective forward stepping.
1,2
The pathophysiology underly-
ing gait impairments in PD and FOG in particular is complex and in-
volves dysfunction of several supraspinal structures in the locomotor
network, including the basal ganglia.
2
The degree of basal ganglia
dysfunction in an individual with PD is not equally distributed across
the various components of the basal ganglia; the loss of dopamin-
ergic innervation and therefore dysfunction is greatest in the pos-
terior putamen,
3
a region that is associated with the control of au-
tomatized (or habitual) behavior.
4
In contrast, dopaminergic
innervation to the rostromedial striatum, a region that is primarily
involved in the production of goal-directed movements, is rela-
tively spared.
4
Translated to gait, this means that patients with PD
may experience difficulties walking in an automatic manner (ie, with-
out consciously paying attention to it). As a consequence, patients
must progressively rely on a goal-directed control of their gait. This
goal-directed control of movements is possible in the presence of a
clear external stimulus because patients find it difficult to inter-
nally generate movements (ie, producing identical movementsin the
absence of an external cue).
5
In addition to basal ganglia dysfunction, disturbances in other
parts of the locomotor network, including cortical regions (eg, fron-
tal cortices involved in executive functions), midbrain locomotor re-
gions, and brain stem structures, contribute to gait disturbances in
PD as well.
2,6
This implies that patients not only manifest a re-
duced automaticity of walking but also experience other problems,
such as difficulties to produce adequate postural adjustments nec-
essary for walking in a safe and efficient manner.Also, cognitive defi-
cits influence gait dysfunction and the regularity of walking.
7
In ad-
dition, cognitive dysfunction may also hamper an efficient switching
from habitual to goal-directed gait control.
8
IMPORTANCE Patients with Parkinson disease can use a wide variety of strategies to
compensate for their gait impairments. Examples include walking while rhythmically
bouncing a ball, crossing the legs when walking, or stepping over an inverted cane. An
overview and classification of the many available compensation strategies may contribute to
understanding their underlying mechanisms and developing focused rehabilitation
techniques. Moreover, a comprehensive summary of compensation strategies may help
patients by allowing them to select a strategy that best matches their needs and preferences
and health care professionals by permitting them to incorporate these into their therapeutic
arsenal. To create this overview, this narrative review discusses collected video recordings of
patients who spontaneously informed clinicians about the use of self-invented tricks and aids
to improve their mobility.
OBSERVATIONS Fifty-nine unique compensation strategies were identified from
approximately several hundred videos. Here, these observed strategies are classified into
7 main categories for elaboration on their possible underlying mechanisms. The overarching
working mechanisms involve an allocation of attention to gait, the introduction of goal
directedness, and the use of motor programs that are less automatized than those used for
normal walking.
CONCLUSIONS AND RELEVANCE Overall, these compensation strategies seem to appeal to
processes that refer to earlier phases of the motor learning process rather than to a reliance
on final consolidation. This review discusses the implications of the various compensation
strategies for the management of gait impairment in Parkinson disease.
JAMA Neurol. doi:10.1001/jamaneurol.2019.0033
Published online March 25, 2019.
Video
Author Affiliations: Author
affiliations are listed at the end of this
article.
Corresponding Author: Jorik
Nonnekes, MD, PhD, Radboud
University Medical Centre,
PO Box 9101, 6500 HB Nijmegen,
the Netherlands (jorik.nonnekes@
radboudumc.nl).
Clinical Review & Education
JAMA Neurology | Review
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Patients with PD often spontaneously use a variety of strate-
gies to compensate for their suboptimal control of locomotion.
Examples include walking while rhythmically bouncing a ball,
crossing the legs when walking, or counting while they are walk-
ing. Such strategies are aimed both at maintaining an optimal gait
pattern (preventing gait decline) and regaining a more normal
gait pattern once an episode of FOG has occurred. Several com-
pensation strategies have been described in the literature,
9-13
typically on an anecdotal basis, but a comprehensive overview
and classification of available strategies is currently lacking, to our
knowledge. Such an overview is important, because analyzing
common traits of compensation strategies may contribute to
understanding their underlying mechanisms and developing
focused rehabilitation techniques. Moreover, a comprehensive
summary of compensation strategies may serve as a source of
inspiration for patients, allowing them to select a strategy that
best matches their personal needs and preferences and health
care professionals to now incorporate this repertoire into their
therapeutic arsenal. Finally, we see this article as something of a
tribute to the patients’ impressive creativity, resilience, and intrin-
sic motivation to cope with their disease.
Methods
To provide an overview of the available compensation strategies
for gait impairments in individuals with PD, we collected video
recordings of patients who had spontaneously informed us about
the use of self-invented tricks and aids to improve their mobility.
Specifically, we asked them to bring home videos showing the
strategies they were using to walk indoors or outdoors. In some
cases, additional videos were recorded during the patients’ visits
in the consulting room or hospital. Moreover, we searched our
personal video databases for videos of patients with PD who used
compensation strategies to overcome their gait deficits. Finally,
we performed a literature search of PubMed to identify further
anecdotal examples, using the following search terms: gait,Par-
kinson,parkinsonism,treatment,compensation, and cueing.Over
a period of 4 years, we collected 59 unique compensation strate-
gies from several hundred videos (without counting all videos
retrieved and viewed). We stopped our search strategy when we
felt that data saturation had been reached.
Many strategies appeared to resort to 1 of several basic com-
pensation mechanisms. Using the available literature and our
clinical experience, we reached agreement on a classification
scheme for compensation strategies for gait deficits in patients
with PD (Table 1). This classification scheme entails 7 main cat-
egories of compensation strategies, which are thought to have a
different underlying working mechanism. After constructing the
classification scheme during a face-to-face discussion, we subse-
quently reached consensus during a series of teleconferences on
classification of each collected video into these predefined com-
pensation categories (Table 2). Here, we will elaborate on the
observed strategies and possible underlying working mechanisms
and their implication for the management of gait impairments in
individuals with PD.
Classification of Compensation Strategies
External Cueing
The first main compensation strategy involves cueing. External cues
are perhaps the most commonly known compensation strategy for
gait impairments in individuals with PD, and this is reflected by the
large number of videos that we collected that all showed some form
of external cueing. We collected 26 unique strategies (44%of all 59
strategies) involving a form of externalcueing (Table 2). External cues
refer to meaningful auditory, proprioceptive, or visual stimuli that
Table 1. Classification of Compensation Strategies for Gait Impairments
in Parkinson Disease and Their Possible Working Mechanism
Compensation
Strategy Principal Mechanism Phenomenology
Restoring
walking
Using external
cues
External stimuli provide a
movement reference or target,
which introduces goal-directed
behavior and may initiate
cortically generated movements
by bypassing automatic motor
control. Rhythmicity and
sensory cues might be valuable.
Sensory cues may theoretically
also assist in filtering
information and prioritizing
tasks, especially during response
selection under conflict
(improving executive attention).
Using auditory cues,
typically rhythmic;
single or rhythmic,
2-dimensional or
3-dimensional visual
cues; or somatosensory
cues, often rhythmic
Using internal
cues
Acts as single cue or trigger for
start, not as a continuous cue.
Helps to achieve focused
attention toward specific
components of gait, to shift
automatic motor control into a
goal-directed one.
Focusing on
predetermined
components of gait;
mental arithmetic or
self-prompting
Changing
balance
requirements
Facilitates ability to make lateral
weight shifts, thereby easing the
swing phase of the unloaded leg,
particularly in gait initiation,
turning, or approaching.
Narrowing the base of
support; shifting
weight in place prior to
stepping; making wider
turns; using walking
aids or supported
walking
Altering the
mental state
Enhancing general alertness and
arousal. This may help to shift
automatic motor control to a
goal-directed one.
Limiting anxiety or fear
of falling; increasing
motivation;
experiencing kinesia
paradoxa
Motor imagery
or action
observation
Both processes involve
activation of the mirror neuron
system, simulate the real action,
and can be considered as offline
operations of the motor system.
It might help to generate
cortically generated movement
more directly.
NA
New walking
pattern
Using alternate motor programs
less overlearned and less
dependent on automatized
generation by the basal ganglia,
since walking difficulty might be
a task-specific problem.
Changing the straight
gait pattern (eg,
scissoring, skating
movements, knee
lifting); using other
forms of locomotion
(eg, jumping, running,
backward walking)
Alternatives to
normal walking
Other forms of
using the legs
to move
forward
Examples include bicycling,
ice skating, and crawling.
NA
Mixed methods Variable combination of other
mechanisms.
NA
Abbreviation: NA, not applicable.
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invigorate and facilitate motor sequences.
14
These external stimuli
provide a movement reference or target that is most likely predic-
tive in nature.
15
Examples include walking at the rhythm of a
metronome,
1
stepping over 2-dimensional or 3-dimensional visual
cues placed in a regular pattern on the floor,
11
and stepping over a
laser beam (projected via a walker,belt , stick,or shoe). The benefi-
cial effects of external cueing are endorsed by a review on external
cueing that included studies with FOG as primary or secondary
outcome.
16
In 6 of 10 studies, online auditory or visual cueing ap-
plied during ongoing gait reduced FOG in patients in the off-
medication state. The 4 negative studies were conducted while pa-
tients were on-medication, suggesting that cues were either not
effective when patients used their dopaminergic medication or,most
likely, that the statistical power was too low in this disease state to
Table 2. Video-IllustratedCompensation Strategies and Possible
Underlying Mechanisms
Compensation Strategy Possible Underlying Mechanism
a
Walking while rhythmically bouncing
a basketball or tennis ball
Auditory cues, somatosensory cues,
other forms of locomotion
Boulder hopping (jumping from
stone to stone)
Visual cues, other forms of locomotion
Stepping over an inverted cane Visual cues
Pressing temples with index fingers
b
Somatosensory cues, focusing on
predetermined components of gait,
and motor imagery or action
observation
Moving forward as if ice skating
b
Change of the straight gait pattern
Lifting the knees very high Change of the straight gait pattern
Holding the belt with both hands Somatosensory cues
Improvement of gait when fencing Increasing motivation, kinesia
paradoxa, other forms of locomotion
Walking with a weight in each hand Somatosensory cues
Upholding a football Visual cues, other forms of locomotion
Jumping Other forms of locomotion
Moving forward using a walk-bicycle Walking aids or supported walking
Ice skating Other forms of using the legs to move
forward
Walking on a painted staircase
illusion
Visual cues
Kicking a cane or a stick Visual cues, change of the straight gait
pattern
Walking sideways
b
Other forms of locomotion
Making movements as if being a
toreador
Increasing motivation, kinesia
paradoxa, other forms of locomotion
Stepping over a laser beam projected
via a belt, stick, or shoes
Visual cues
Cycling
b
Other forms of using the legs to move
forward
Walking at the rhythm of a
metronome
b
Auditory cues
Crossing the legs when walking Change of the straight gait pattern
Walking with very large steps Change of the straight gait pattern
Walking at the rhythm of music Auditory cues
2-Dimensional visual cues placed in a
regular pattern on the floor
Visual cues
3-Dimensional visual cues placed in a
regular pattern on the floor
b
Visual cues
Walking in water Changing balance requirements
Watching another person walking
before gait initiation in real life or via
smartglasses
Motor imagery or action observation
Improvement of gait when playing
badminton
Other forms of locomotion
Moving forward while dancing Auditory cues, other forms of
locomotion
Making wider turns Changing balance requirements
Kicking a ball attached with a cord to
the patients hand
Visual cues, change of the straight gait
pattern
Jumping and running while playing
basketball
Visual cues, increasing motivation,
other forms of locomotion
Starting gait after having brought
the arms behind the back
Focusing on predetermined
components of gait
Feeling stable with cutaneous
vibrations
Somatosensory cues
Improvement of freezing of gait
under rhythmic paresthesias induced
by spinal cord stimulation
Somatosensory cues
Walking with weights on the shoes Somatosensory cues
(continued)
Table 2. Video-IllustratedCompensation Strategies and Possible
Underlying Mechanisms (continued)
Compensation Strategy Possible Underlying Mechanism
a
Walking along a narrow beam Visual cues, narrowing the base of
support, increasing motivation, change
of the straight gait pattern
Mounting and descending a ladder Somatosensory cues, other forms of
locomotion
Running
b
Other forms of locomotion
Riding a scooter
b
Other forms of using the legs to move
forward
Roller skating Other forms of using the legs to move
forward
Walking upstairs Visual cues, other forms of locomotion
Walking downstairs Visual cues, other forms of locomotion
Walking on stilts Other forms of locomotion
Kicking an object that is sliding
forward on the floor
Visual cues, change of the straight gait
pattern
Gliding feet on a smooth floor Change of the straight gait pattern
Jumping forward with propping both
arms upon handrails
Other forms of locomotion
Making sidestep before stepping
forward
Change of the straight gait pattern
Walking after lifting body weight
while sitting on the floor
Increasing motivation
Walking after tensing trunk muscles
by bending backward
Focusing on predetermined
components of gait, increasing
motivation
Walking after tensing lower limbs Focusing on predetermined
components of gait, increasing
motivation
Walking backward Other forms of locomotion
Stepping over someone else's foot to
initiate walking
Visual cues
Stepping over own foot to initiate
walking
Visual cues, focusing on predetermined
components of gait, narrowing the
base of support, change of the straight
gait pattern
Weight shifting in place before gait
initiation
Weight shifts in place prior to stepping
Turning with medial shift of base of
support by lifting the arm
Narrowing the base of support, change
of the straight gait pattern
Making a heel strike at every count
b
Focusing on predetermined
components of gait
Turning while thinking about better
weight shift
Focusing on predetermined
components of gait
a
Terms used in the Category column occur in Table 1.
b
See Video.
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be able to detect a meaningful change. The response to cueing usu-
ally depends on the type of external cue; spatial (visual) cues cor-
rect and regulate the scaling and amplitude generation during walk-
ing, whereas temporal (auditory) cues facilitate gait timing and
interlimb coordination.
17,18
The mechanisms underlying external cueing might be 2-fold.
First, external cues introduce goal-directed behavior,which circum-
navigate those parts of the basal ganglia that are involved in au-
tomatized motor control and rely on regions of the basal ganglia that
are less severely affected by loss of dopaminergic innvervation.
4
Goal-directed control of movements in PD generally improves in the
presence of external stimuli,
5
which might explain why external cues
are so often used.
19,20
The exact neural networks involved in re-
stored response generation using external stimuli have to be unrav-
eled by future studies, but compensation might involve the cerebel-
lum, the superior parietal cortex, and dorsal premotor cortex, besides
the rostromedial striatum involved in goal-directed behavior.
21,22
A second working mechanism might be that cues assist in filtering
information and prioritizing a stimulus, especially during response
selection under conflict (which is often the case in the complex real-
life world). Control of gait is not just dependent on motor circuit-
ries but also on intact executive function, which is regulated by the
frontostriatal circuitry. Patients with PD who experience FOG of-
ten display executive dysfunction, resulting in difficulties in re-
sponse selection under conflict.
20
External cues might compen-
sate for this deficit and improve executiveattention a hypothesis that
is supported by the robust finding that auditory cueing is beneficial
during dual tasking.
23,24
Internal Cueing
Patients can also use internal cues to compensate for their gait
impairments.
13
In keeping with the concept that gait impairments
in PD are partly owing to an automaticity deficit, behavioral strate-
gies are needed to shift patients’ automatic motor control to a goal-
directed one.
4
Rather than being guided by external input, pa-
tients can also use internal cues to orient or focus attention toward
gait by using specific self-prompting instructions
13,25
or concentrat-
ing on predetermined components of gait (eg, making a heel strike
at every count [Video]). Orienting is thought to involve prefrontal
areas (frontal eye fields) and parietal areas.
26
Obviously, these com-
pensation strategies are not visible on videos, but patients fre-
quently report to use these internal compensation strategies.
13
Some patients also use tricks that help them to allocate their at-
tention to gait, and these tricks can be seen on a video. Examples
include a patient that pressed his index fingers against his temples
before gait initiation,
9
a patient that started gait after having brought
his arms behind his back, and a patient that tensed his trunk muscles
by bending backward before starting to walk.
Motor Imagery and Action Observation
Motor imagery and action observation are compensation strate-
gies that at first sight seem to be a form of internal cueing. How-
ever, both processes differ from internal cueing as they stimulate,
to some degree, the real action including all its components.
27,28
They
can be considered as offline operations of the motor system, which
is not the case during internal cueing. During action observation, a
patient observes someone else walking, whereas during motor im-
agery, the patient rehearses and imagines to carry out the full mo-
tor act (in this case walking) in the absence of overt motor output.
29
Motor imagery and action observation likely compensate for re-
duced automaticity by mental simulation
30
or visualization of the
action of gait without its actual execution. Both compensation strat-
egies imply activation of the mirror neuron system
31
and involve the
supplementary motor area, the dorsal premotor cortex, the supra-
marginal gyrus, and the superior parietal lobe.
32
However, thereare
also several nonoverlapping regions involved, which indicate that
motor imagery and action observation are clearly distinct phenom-
ena. For example, motor imagery has been associated with activa-
tion of the ventral premotor cortex, whereas action observation has
been associated with additional activation located in the temporal
pathways.
33
Altering the Mental State
Alteration of the mental state is another compensation strategy that
might help shift to a goal-directed mode of control. In extreme forms,
this is observed during paradoxical kinesia, which is defined as the
sudden transient ability of patients with PD to perform a task they
were previously unable to perform, usually when facing an imme-
diate threat.
34
A classic example is the patients’ marked improve-
ment of gait directly after an earthquake.
35
Obviously, paradoxical
kinesia cannot be used as a compensation strategy on a daily basis.
However,improvements of gait impairments owing to increased mo-
tivation might have a similar working mechanism, involving an en-
hancement of alertness or arousal. Importantly, altering the men-
tal state does not have the same working mechanism as internal
cueing; internal cueing is thought to achieve focused attention to-
ward specific aspects of gait, whereas an alteration of the mental
state results in a more generic increase in attention. This alerting role
of attention is thought to involve activation of the noradrenergicne t-
work in thalamic, frontal, and parietal areas
26
and cholinergic cor-
ticopetal networks.
36
With respect to paradoxical kinesia, it has also
been suggested that the working mechanism could involve a burst
of dopamine release from basal ganglia reserves, thus restoring au-
tomaticity and self-initiation of movements.
34
Alternatively, para-
doxical kinesia may, at least some of the time, also be because of a
shift to external control (for example, when throwing a ball at a pa-
tient, who then can suddenly lift the arms).
Changing the Balance Requirements
Another compensation strategy involves a change of balance re-
quirements during gait. In contrast with the compensation strate-
gies described above, most of these motor strategies do not target
a change of the neural circuits involved in the production of gait, but
rather adapt walking such that the postural demands are reduced.
This is needed as patients with PD and especially those with FOG
can have difficulties to make an appropriate lateral weight shift onto
the stance leg preceding a step to unload the stepping leg. Such an-
ticipatory postural adjustments have been identified during gait ini-
tiation using force plates and are frequently too small in patients with
PD.
37-39
However, small anticipatory postural adjustments are pre-
sumably not the cause of FOG, because these postural adjust-
ments have been reported to be larger during trials of individuals
with FOG compared with trials of individuals without FOG.
39
More
likely, patients may have difficulties integrating the weight shift with
the ensuing step, possibly resulting in FOG with alternating trem-
bling of the legs.
40,41
Reduced postural adjustments have been at-
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tributed to reduced brain activity in the supplementary motor
area,
42,43
whereas difficulties in integrating postural adjustments
with subsequent steps might be owing to dysfunction at the level
of the pedunculopontine nucleus and pontomedullary reticular
formation.
44,45
Several strategies compensate for dysfunction of
these structures by reducing the need to make a lateral weight shift
or by facilitating the integration between posturaladjustments and
steps. We collected 7 unique compensation strategies that in-
volved a change of the balance requirements. One common ap-
plied strategy is to make wider rather than narrow turns, which pre-
sumably facilitates the integration between weight shifts and steps
compared with the more delicate integration when making a nar-
row turn. Another example is the use of a walk-bicycle, which is a
specific bicycle without pedals and a low seat that allows stepping
movements without the need for generating posturaladjustments.
46
In fact, 1 of various explanations why many patients with FOG can
still ride a bicycle with considerably fewer difficulties is also associ-
ated with this weight shifting, which is not needed when patients
are seated on their buttocks.
47
Adapting a New Bipedal Locomotor Pattern or Using
Alternatives for Walking
Another category of compensation strategies is the adoption of a
new walking pattern. A new walking pattern uses alternative mo-
tor programs that are less overlearned than those involved in nor-
mal walking and therefore less dependent on automatic genera-
tion by the basal ganglia. Usually, these movements are not
completely new but have been learned previously; associated mo-
tor programs have been consolidated but refer to earlier phases of
the motor learning process rather than to a reliance on final consoli-
dation. We have collected 28 unique videos of patients who had al-
tered their normal walking pattern. Examples include patients who
lift their knees very high or walk as if they are ice skating (Video). In
addition to these relatively small adaptions, we have also observed
large adaptations of the normal walking pattern, such as a patient
who was unable to walk forward but could walk backward, and pa-
tients who showed an improved gait pattern when walking side-
ways (a so-called crab walk; Video) or running (Video). Runningand
walking sideways or backward is presumably less overlearned than
normal walking. This hypothesis is supported by observations in pa-
tients with dystonia, another movement disorder involvingdysfunc-
tion of the basal ganglia,
48
in which abnormal postures are often ob-
served during walking but not running or walking backward.
49
Other Forms of Using the Legs to Move Forward
Yet another compensation category, one that is somehow associ-
ated with the adaption of a new walking pattern, involvesother forms
of using the legs to move forward. An already classic illustration is
the preserved ability of many patients to ride a bicycle (Video),
10
which appears to be a common phenomenon in countries where cy-
cling is prevalent.
50
Others examples are patients who are able to
ice skate or ride a scooter (Video) without any problems, despite im-
pairments during walking. For an extensive discussion of all pos-
sible mechanisms underlying the preserved ability to cycle in pa-
tients with PD, we refer to a viewpoint article by Snijders et al.
47
One
possibility is that the motor system is organized according to tasks,
and some of these tasks, such as walking, are affected by PD,whereas
others, such as ice skating or riding a bicycle, are not affected. This
might be associated with the prior amount of learning, suggesting
that cycling and ice skating are less overlearned than walking. An-
other hypothesis is that during these alternative movements, a dif-
ferent control mode of repetitive cycles is required, which is driven
by external cueing (bicycling) or attentional control (ice skating). As
mentioned, there is less need to create lateral weight shifts during
cycling than walking. Moreover, the pedals are usually coupled, which
restores the symmetry of leg movements in this typically asymmet-
ric disease. In contrast, during real or mimicked ice skating, large lat-
eral weight shifts are essential to prevent a fall. This explicit urge to
make a large lateral weight shift to prevent a fall might explain why
some patients are inclined to use this strategy.
Combination of Compensation Strategies
Nineteen videos may have involved a combination of the aforemen-
tioned working mechanisms. One example is a patient who showed a
significant improvement of his gait pattern when rhythmically bounc-
ing a ball (Video). Rhythmically bouncing ball could act as a rhythmi-
cal auditory or somatosensory cue, but it may also trigger an alterna-
tive motor program that is less overlearned and therefore less depen-
dent on automatic generation by the basal ganglia. Another commonly
applied strategy is to purposely walk with a narrow base of support,
which is typically seen in many patients with PD.
51
One may argue that
this requires smaller postural adjustments compared with gait with a
normal-to-wide stance width. However, it might also require alterna-
tive motor programs that are less overlearned than those involvedin
normal walking or involve a combination of both mechanisms. A final
example of combined compensation strategies is the markedimprove-
ment of gait when climbing a staircase (Video). In the various videos
that we collected, it seems that this is mainly beneficial when there is
a large contrast between the separate steps of the stairway,
12
suggest-
ing that the stairs serve as a 3-dimensional visual cue. However,another
plausible explanation is that that climbing stairs involves a motor pro-
gram that is less overlearned than normal walking. In addition, stairs
could force patients to produce a more effective lateral weight shift to
avoid stumbling.
Conclusions and Future Directions
The collected variety of compensation strategies highlights the enor-
mous inventiveness of patients and their caregivers and underscores
the need to collaborate with them to refine current treatment ap-
proaches. Overarching working mechanisms of compensation strat-
egies seem to involve an allocation of attention to gait, the introduc-
tion of goal directedness, and the use of motor programs that are less
overlearned than those used in normal walking. Overall, these strat-
egies seem to appeal to processes that refer to earlier phases of the mo-
tor learning process rather than to a reliance on final consolidation.
An additional overarching working mechanism of all compensa-
tion strategies might be the reduction of anxiety.There is an increas-
ing line of evidence that shows that anxiety is associated with FOG,
52-55
although it is still debated whether it plays a causal or modifying role.
Several patients spontaneously reported that use of a compensation
strategy reduced their fear to freeze, as it providedthem with a backup
plan. One example is a patient who showed a marked improvementof
his gait pattern when walking with laser shoes,
56
although he actually
did not look at the projected laser beams. When debriefed about this,
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he told us that he indeed did not look at the cues for most of the time,
but that he simply felt more comfortable having the laser shoes with
him just in case.
Importantly,compensation strategies do not have the same ef-
fect in each individual patient and can sometimes also exaggerate
gait impairments. This suggests that each supraspinal structure in-
volved in the locomotion network is not affected to the same ex-
tent in each patient and the reduced neural reserve in patients with
gait impairments creates a thin line between compensation-
induced benefits as well as disturbances.
57
Translatedto clinical prac-
tice, this implies that all patients with PD should be educated about
the available compensation strategies, and that, together with an
experienced therapist, the optimal compensation strategies for that
specific individual should be identified. Such evaluations should not
be limited to 1 occasion but must be repeated if the chosen strate-
gies lose their effectiveness over time.
The reason for a possible reduction or loss of effectiveness of a
particular compensation strategy might be 2-fold. First, the neural
circuitry involved in the compensation strategy may also become
affected by the underlying process of neurodegeneration. Second,
when used frequently, compensation strategies can lose their effi-
cacy when they become increasingly automated themselves, but this
interesting hypothesis needs to be addressed by future studies.
This framework needs to be confirmed by future studies that
further explore the underlying working mechanisms. Future work
is also needed to improve the application of compensation strate-
gies in daily life. A challenge is to now deliver external cueing
safely and on demand in a user-friendly and effective manner
in the patient’s own natural environment. This requires the devel-
opment of wearable sensors that can signal when gait
deteriorates.
58
Recent work on such wearables is promising, but
refinement is needed.
59
Moreover, recent technological advances
improve the ability to provide external cueing in daily-life
situations.
60,61
Examples include wearable minicomputers in the
form of smart glasses to provide rhythmic visual cueing or aug-
mented visual cues on top of the patient’s visual field.
60,62
Another example is the laser shoe, which consists of a shoe
equipped with a transverse line–generating laser mounted on the
front tip, presenting horizontal lines to step over.
56,63
Different
technological advancements may extend the use of other com-
pensation strategies to daily life as well. Examples include the
walk-bicycle
46
and smart glasses showing footages of someone
walking, allowing action observation. Another example is the
CuPiD system (University of Bologna), in which inertial measure-
ment units combined with a smartphone application provide
patients auditory real-time feedback on their gait-performance.
64
A challenge is to translate these new technological advancements
into daily clinical practice, determine their clinical efficacy, and
provide them to patients in combination with more conventional
compensation strategies.
ARTICLE INFORMATION
Accepted for Publication: December 21, 2018.
Published Online: March 25, 2019.
doi:10.1001/jamaneurol.2019.0033
Author Affiliations: Donders Institute for Brain,
Cognition and Behaviour, Department of
Rehabilitation, Radboud University Medical Centre,
Nijmegen, the Netherlands (Nonnekes);
Department of Rehabilitation, Sint Maartenskliniek,
Nijmegen, the Netherlands (Nonnekes); Centre of
Clinical Neuroscience, Department of Neurology,
First Faculty of Medicine, General University
Hospital, Charles University in Prague, Prague,
Czech Republic (Růžička); Department of
Rehabilitation Sciences, Katholieke Universiteit
Leuven, Tervuursevest, Belgium (Nieuwboer);
National Institute of Neurological Disorders and
Stroke, Bethesda, Maryland (Hallett); Edmond J.
Safra Program in Parkinson’s Disease, Morton and
Gloria Shulman Movement Disorders Clinic, Krembil
Research Institute, Division of Neurology,Toronto
Western Hospital, University of Toronto, Toronto,
Ontario, Canada (Fasano); Krembil Brain Institute,
Toronto,Ontario, Canada (Fasano); Donders
Institute for Brain, Cognition and Behaviour,
Department of Neurology, Radboud University
Medical Centre, Nijmegen,
the Netherlands (Bloem).
Author Contributions: Dr Nonnekes had full access
to all of the data in the study and takes responsibility
for the integrity of the data and the accuracy of the
data analysis.
Concept and design: All authors.
Acquisition, analysis, or interpretation of data:
Nonnekes, Ruzicka, Nieuwboer,Hallett, Bloem.
Drafting of the manuscript: Nonnekes, Nieuwboer.
Critical revision of the manuscript for important
intellectual content: Ruzicka, Nieuwboer, Hallett,
Fasano, Bloem.
Administrative, technical, or material support:
Nonnekes.
Supervision: Fasano, Bloem.
Conflict of Interest Disclosures: Dr Bloem reports
grants from the Michael J. FoxFoundation, ZonMw,
Stichting Parkinson Nederland, Parkinson
Vereniging, Hersenstichting Nederland, Parkinson’s
Foundation, Verily Life Sciences, Horizon 2020, and
Topsector Life Sciences and Health; grants and
personal fees from UCB; and personal fees from
Abbvie, Bial, and Zambon, outside the submitted
work. Dr Fasano reports grants, personal fees, and
nonfinancial support from Abbvie, Boston
Scientific, amd Medtronic; grants and personal fees
from Sunovion; and personal fees from Ipsen and
Chiesi, outside the submitted work. Dr Nonnekes
reports a grant from the Michael J. Fox Foundation
and personal fees from Ipsen outside the submitted
work. No other disclosures were reported.
Funder/Sponsor: This studywas supported by
ZonMW Veni (grant 16.196.022[Dr Nonnekes]).
Role of the Funder/Sponsor:The funder had no
role in the design and conduct of the study;
collection, management, analysis, and
interpretation of the data; preparation, review, or
approval of the manuscript; and decision to submit
the manuscript for publication.
Additional Contributions: We thank Peter
Valkovic, MD,PhD, Second Department of
Neurology, Faculty of Medicine, Comenius
University,and Peter Praamstra, MD, PhD, and Bart
van de Warrenburg, MD, PhD, Donders Institute for
Brain, Cognition and Behaviour, Department of
Neurology, Radboud UniversityMedical Centre, for
contributing videos. They were not compensated
for these contributions.
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