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Delaying Mobility Disability in People With Parkinson

Disease Using a Sensorimotor Agility Exercise


Program
Laurie A King and Fay B Horak
PHYS THER. 2009; 89:384-393.
Originally published online February 19, 2009
doi: 10.2522/ptj.20080214

The online version of this article, along with updated information and services, can be
found online at: http://ptjournal.apta.org/content/89/4/384

Collections This article, along with others on similar topics, appears


in the following collection(s):
Gait and Locomotion Training
Gait Disorders
Health and Wellness/Prevention
Parkinson Disease and Parkinsonian Disorders
Perspectives
Therapeutic Exercise
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Perspective

Delaying Mobility Disability in People


With Parkinson Disease Using a
Sensorimotor Agility Exercise Program
Laurie A King, Fay B Horak
LA King, PT, PhD, is Post-doctoral
Fellow, Oregon Health and
Sciences University, Portland, This article introduces a new framework for therapists to develop an exercise
Oregon. program to delay mobility disability in people with Parkinson disease (PD). Mobility,
or the ability to efficiently navigate and function in a variety of environments, requires
FB Horak, PT, PhD, is Research
Professor of Neurology and Ad- balance, agility, and flexibility, all of which are affected by PD. This article summa-
junct Professor of Physiology and rizes recent research identifying how constraints on mobility specific to PD, such as
Biomedical Engineering, Depart- rigidity, bradykinesia, freezing, poor sensory integration, inflexible program selec-
ment of Neurology, Oregon tion, and impaired cognitive processing, limit mobility in people with PD. Based on
Health and Sciences University, these constraints, a conceptual framework for exercises to maintain and improve
West Campus, Building 1, 505
NW 185th Ave, Beaverton, OR mobility is presented. An example of a constraint-focused agility exercise program,
97006-3499 (USA). Address all incorporating movement principles from tai chi, kayaking, boxing, lunges, agility
correspondence to Dr Horak at: training, and Pilates exercises, is presented. This new constraint-focused agility
horakf@ohsu.edu. exercise program is based on a strong scientific framework and includes progressive
[King LA, Horak FB. Delaying mo- levels of sensorimotor, resistance, and coordination challenges that can be custom-
bility disability in people with Par- ized for each patient while maintaining fidelity. Principles for improving mobility
kinson disease using a sensorimo- presented here can be incorporated into an ongoing or long-term exercise program
tor agility exercise program. Phys for people with PD.
Ther. 2009;89:384 –393.]

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A Sensorimotor Agility Exercise Program for People With Parkinson Disease

M
ost people who are diag- that the basal ganglia are critical for Why Exercise May Prevent
nosed with Parkinson dis- sensorimotor agility.2 Critical as- or Delay Mobility Disability
ease (PD) do not consult pects of mobility disability in people in People With PD
with a physical therapist until they with PD, such as postural instability, Exciting new findings in neuro-
already have obvious mobility prob- are unresponsive to pharmacological science regarding the effects of ex-
lems. However, it is possible that a and surgical therapies,7 making pre- ercise on neural plasticity and neu-
rigorous exercise program that fo- ventative exercise an attractive op- roprotection of the brain against
cuses on anticipated problems, tion. As yet, there is no known on- neural degeneration suggest that an
which are inevitable with progres- going exercise program for people intense exercise program can im-
sion of the disease, may help patients diagnosed with PD that focuses on prove brain function in patients with
who do not yet exhibit mobility maintaining or improving their agil- neurological disorders. Specifically,
problems. Although there are excel- ity to slow or reduce their decline in animal studies have demonstrated
lent guidelines for physical thera- mobility. neurogenesis,8 an increase in dopa-
pists to treat patients with PD who mine synthesis and release,9 and in-
exhibit mobility problems in order This article uses the known sensori- creased dopamine in the striatum fol-
to improve or maintain their mobili- motor impairments of PD that affect lowing acute bouts of exercise.10
ty,1,2 there is little research on balance, gait, and postural transi- Such changes in the brain may affect
whether exercise may delay or re- tions to develop a conceptual frame- behavioral recovery as a result of
duce the eventual mobility disability work to design exercises that aim to neuroplasticity (the ability of the
in patients diagnosed with PD. delay disability and maintain or im- brain to make new synaptic connec-
prove mobility in people with PD. tions), neuroprotection, and slowing
The major cause of disability in peo- This framework is based on the cur- of neural degeneration.11,12 Studies
ple with PD is impaired mobility.3 rent knowledge of the neurophysi- with parkinsonian rats have sug-
Mobility, the ability of a person to ology of PD and the inevitable con- gested that chronic exercise may
move safely in a variety of environ- straints on mobility resulting from help reverse motor deficits in ani-
ments in order to accomplish func- basal ganglia degeneration. The sci- mals by changing brain function.
tional tasks,4 requires dynamic neu- entifically based principles presented Specifically, rats that ran on a tread-
ral control to quickly and effectively here, which are focused on mobility mill showed preservation of dopami-
adapt locomotion, balance, and pos- disorders in people with PD, can be nergic cell bodies and terminals11,13
tural transitions to changing environ- incorporated into an existing ther- associated with improved running
mental and task conditions. Such dy- apy program for people with PD. distance and speed,12 indicating a
namic control requires sensorimotor neuroprotective effect of exercise.
agility, which involves coordination Based on this framework, this article Conversely, nonuse of a limb in-
of complex sequences of move- also presents an example of a novel duced by casting in parkinsonian rats
ments, ongoing evaluation of envi- sensorimotor agility program that we increased motor deficits as well as
ronmental cues and contexts, the are currently testing in a clinical trial. loss of dopaminergic terminals.11
ability to quickly switch motor pro- This program is unique in that it en- Aerobic exercise, such as treadmill
grams when environmental condi- courages a partnership among phys- training and walking programs, has
tions change, and the ability to main- ical therapists, exercise trainers, and been tested in individuals with PD
tain safe mobility during multiple patients to set up, progress, and re- and has been shown to improve gait
motor and cognitive tasks.5,6 The evaluate an exercise program that ul- parameters, quality of life, and leva-
types of mobility deficits inevitable timately can be carried out indepen- dopa efficacy.14 –16 However, it is not
with the progression of PD suggest dently in the community. It is likely clear whether aerobic training, by
that a mobility program, such as the itself, is the best approach to improv-
one presented here, would need to ing mobility, which depends upon
Available With be sustained and modified through- dynamic balance, dual tasking, nego-
This Article at out the course of the disease to main- tiating complex environments, quick
www.ptjournal.org tain maximal benefit. changes in movement direction, and
other sensorimotor skills affected by
• Audio Abstracts Podcast PD. It is possible that treadmill train-
This article was published ahead of ing, for example, could be even
print on February 19, 2009, at more effective for addressing com-
www.ptjournal.org. plex mobility issues for people with

April 2009 Volume 89 Number 4 Physical Therapy f 385


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A Sensorimotor Agility Exercise Program for People With Parkinson Disease

PD if the therapist could incorporate challenges into a comprehensive ex- Constraints Affecting
tasks such as dual tasking, balance ercise program directed at delaying Mobility in People With PD,
training, and set-switching into a and reducing mobility problems in With Implications for the
treadmill program. individuals with PD.
Sensorimotor Agility
There currently are many untested Reduce Mobility Program
exercise programs available for peo- Constraints With Exercise Rigidity
ple with PD17–19 as well as several People with mild or newly diag- Parkinsonian rigidity is characterized
randomized controlled studies that nosed PD often do not have obvious by an increased resistance to passive
test specific exercises, such as muscle weakness or poor balance.43 movement throughout the entire
strength (force-generating capacity) Nevertheless, the literature suggests range of motion, in both agonist and
training or gait training.20 –29 The ap- that muscle weakness, secondary to antagonist muscle groups.55–57 The
proach presented in this article is abnormal muscle activation associ- functional outcomes of rigidity, in
focused on exercises that challenge ated with bradykinesia and rigidity, general, include a flexed posture,58
sensorimotor control of dynamic bal- can be present at all stages of lack of trunk rotation,59,60 and
ance and gait to improve mobility in PD.44 – 47 Similarly, balance and mo- reduced joint range of movement
people with PD. There are many bility problems may be present in during postural transitions and
other aspects of PD that also must be people with mild PD but only be- gait.56,61 Electromyography studies
addressed in rehabilitation. come apparent when more-complex have shown that people with PD
coordination is required under chal- have high tonic background activity,
Drive Neuroplasticity lenging conditions.48,49 For example, especially in the flexors, and co-
With Task-Specific mobility problems may only be ap- contraction of muscles during move-
ment, especially in the axial mus-
Agility Exercise parent when an individual with PD
cles.56,57 In addition, antagonist
Studies in rats have demonstrated is attempting to walk quickly in a
cluttered environment while talking muscle activation is larger and ear-
that task-specific agility training (eg,
on a cell phone. As the disease pro- lier, resulting in coactivation of mus-
acrobatic, environmental enrichment-
gresses, balance problems become cle groups during automatic postural
type, high-beam balance course) re-
more apparent, just as patients begin responses.61
sults in larger improvements in mo-
tor skills as well as larger changes in to show impaired kinesthesia and
inability to quickly change postural Another characteristic of parkinso-
synaptic plasticity than simple, re-
strategies.50,51 The basal ganglia af- nian rigidity is axial rigidity, which
petitive aerobic training such as run-
fect balance and gait by contributing results in a loss of natural vertebral,
ning on treadmills.30 –35 Task-specific
to automaticity, self-initiated gait and pelvis/shoulder girdle, and femur/
exercise also has been shown to be
postural transitions, changing motor pelvis flexibility and range of motion
more effective than aerobic or gen-
programs quickly, sequencing ac- that accompanies efficient postural
eral exercise to improve task perfor-
tions, and using proprioceptive in- and locomotor activities.60,62 Wright
mance in patients with stroke.36,37
formation for kinesthesia and multi- et al55 found that rigidity in the neck,
Task-specific exercises targeted at a
segmental coordination.52–54 During torso, and hips of standing subjects
single, specific balance or gait im-
the progression of PD, mobility is was 3 to 5 times greater in subjects
pairment in patients with PD have
progressively constrained by rigidity, with PD than in age-matched control
been shown to be effective. For
bradykinesia, freezing, sensory inte- subjects when measuring the tor-
example, exercises targeted at im-
gration, inflexible motor program sional resistance to passive move-
proving small step size, poor axial
selection, and attention and cogni- ment along the longitudinal axis dur-
mobility, difficulty with postural
tion.2 Table 1 summarizes con- ing twisting movements. Levodopa
transitions, small movement ampli-
straints on mobility due to PD, the medication did not improve their
tude, or slow speed of compen-
impact of these constraints on mo- axial rigidity.55 The high axial tone
satory stepping have individually
bility, and the goals of exercises that (velocity-dependent resistance to
been shown to be effective in im-
could potentially reduce the impact stretch) in patients with PD contrib-
proving each particular aspect of mo-
of each constraint. utes to their characteristic “en bloc”
bility.18,22,38 – 42 We have borrowed
trunk motions, which make it diffi-
singular techniques from several suc-
cult for them to perform activities
cessful programs and combined them
such as rolling over in bed or turning
with task-specific components of mo-
while walking.62
bility and systematic sensorimotor

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A Sensorimotor Agility Exercise Program for People With Parkinson Disease

Table 1.
Parkinsonian Constraints Affecting Mobility and Exercise Principles Designed to Reduce These Constraintsa

Constraints Impact on Mobility Exercise Principles

I. Rigidity Agonist/antagonist co-contraction Trunk rotation


Flexed alignment of trunk Reciprocal movements
Reduced trunk rotation Rhythmic movements
Reduced joint range of movement Erect alignment
High axial tone (stiffness) Large CoM movements
Increase limits of stability

II. Bradykinesia Slow, small movements Fast, large steps


Narrow base of support CoM control
Lack of arm swing Large arm swings

III. Freezing Poor anticipatory postural adjustments Improve weight shifting


Abnormal mapping of body and movement Understand role of external cues
Abnormal visual-spatial maps Exercise in small spaces
Divided attention affects mobility Practice dual tasks

IV. Inflexible program selection Poor rolling, sit-to-stand maneuvers, turns Plan task in advance
(sequential coordination) Difficult floor transfers Quick change strategies
Inability to change strategy quickly Sequencing components of task

V. Impaired sensory integration Inaccurate without vision Kinesthetic awareness


Imbalance on unstable surface Decrease surface dependence
Poor alignment with environment Flexible orientation

VI. Reduced executive function Difficulty with dual tasks and sequences of actions Practice gait and balance with secondary
and attention task and sequences of actions (ie; boxing,
agility course)
a
CoM⫽center of mass.

Schenkman et al63 showed that ex- Bradykinesia responses in people with PD gener-
ercise can increase trunk flexibility Bradykinesia is most commonly de- ally are not improved by antiparkin-
in people with PD. We propose fined as slowness of voluntary move- sonian medications, highlighting the
an agility program that includes ment,43 but it also is associated with need for an exercise approach to this
movements that minimize agonist- slow and weak postural responses to constraint on mobility.6 Bradykinesia
antagonist muscle co-contraction (ie, perturbations and anticipatory pos- also is seen in postural transitions such
reciprocal movements), promote ax- tural adjustments. Reactive postural as turning70 and the supine-to-stand
ial rotation, lengthen the flexor mus- responses to surface translations61,64 manuever,59 as well as in single-joint
cles, and strengthen the extensor and anticipatory postural movements movements71 and multi-joint reaching
muscles to promote an erect pos- prior to rising onto toes65 and prior movements72 in people with PD.
ture. Rigidity can potentially be ad- to step initiation66 are bradykinetic
dressed with kayaking, an exercise in patients with PD. Bradykinetic vol- Bradykinesia is evident in slowed
in which the person counter-rotates untary stepping and postural com- rate of increase and decrease of mus-
the shoulder and pelvic girdle; tai pensatory stepping are characterized cle activation patterns.73 Reduction
chi, a set of exercises that focuses on by a delayed time to lift the swing in muscle strength in people with PD
the individual’s awareness of pos- limb, a weak push-off, reduced leg lift, has been attributed primarily to re-
tural alignment during postural tran- a small stride length, and lack of arm duced cortical drive to muscles be-
sitions; and pre-Pilates, a series of swing.61,64,66,67 Bradykinesia also is cause voluntary contraction, but not
exercises aimed at increasing spinal apparent in reduced voluntary and muscle response to nerve stimula-
mobility and lengthening flexor mus- reactive limits of stability, especially tion, is weak in these individuals.74,75
cles groups. In addition, the program in the backward direction.64,68 The Electromyographic activity in bradyki-
should include strategies for turning characteristic narrow stance of pa- netic muscles often is fractionated into
and transitioning from a standing po- tients with PD may be compensatory multiple bursts and is not well scaled
sition to sitting on the floor and back for bradykinetic anticipatory postural for changes in movement distance or
again that emphasize trunk and head adjustments prior to a step, at the velocity.71 Years of bradykinesia from
rotation (Tabs. 2 and 3).18 expense of reduced lateral postural abnormal, centrally driven muscle
stability.67,69 Bradykinetic postural control and abnormal, inefficient pat-

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A Sensorimotor Agility Exercise Program for People With Parkinson Disease

Table 2.
Representative Agility Exercise Program, With Progressions

Exercise Actions Progressions

I. Tai chi: Increase limits of stability, Prayer wheel: anterior-posterior slow, rhythmical Learn one action per week, starting with
improve perception of posture and weight shifts coordinated with large arm circles weight shifting and leg placement and
coordination of arms and legs and Cat walk: slow and purposeful steps, with progressing to coordinated arm, neck,
backward and lateral large steps diagonal weight shifts and torso motion
Cloud hands: slow lateral steps, with trunk vertical
Part the wild horse’s mane: coordination of arms
and legs while walking forward
Repulsing the monkey: deliberate slow, backward
walking, with diagonal weight shifts

II. Kayaking: Trunk rotation, Kayaking stroke: diagonal trunk rotation, with Speed, surface, resistance, vision, dual task
segmental coordination, speed reciprocal forward arm extension and backward
arm retraction

III. Agility course: Agility, High knees: high-amplitude stepping, with hand Speed, dual task, quick change in directions,
multisegmental coordination, quick slapping knees tight and cluttered spaces, vision
changes in direction, and mobility Lateral shuffle: quick, lateral steps
in tight spaces Tire course: wide-based, quick and high steps, with
turns
Grapevine cross: over coordinated steps

IV. Boxing: Anticipatory postural Jab: short, straight punch from shoulder Speed, dual task, walking forward, walking
adjustments, postural corrections, Cross: power punch, with trunk rotation, leading backward, turns, remembered sequences
fast arm and foot motions, arm crosses midline of action
backward walking, timing, Hook: short, lateral punch, with elbow bent and
sequencing actions wrist twisted inward, trunk rotation
Combinations: 2 or more punches delivered quickly
after one another

V. Lunges: Big steps, stepping for Postural correction: lean until center of mass is Surface (up and down stool), external cues,
postural correction, limits of outside base of support, requiring a step; all vision, resistance, dual task (add arm
stability, quick changes in directions movements or cognitive task)
direction, internal representation of Single multidirectional steps (clock stepping)
body Dynamic multidirectional lunge walking

VI. Pre-Pilates: Improve trunk control, Cervical range of motion, sit-to-stand maneuver Improve form and speed
axial rotation and extension, Floor transfer, supine (bridging)
functional transitions, sequencing Rolling (prone lying, progress to spinal extension
actions exercises)
Quadruped (bird-dog, cat-camel, thread the
needle)
Half-kneeling to stand

terns of muscle recruitment limit func- lunges, kicks, and quick boxing Freezing
tional mobility and eventually may re- movements. Patients also practice Freezing of gait manifests as a move-
sult in focal muscle weakness. taking large, protective steps while ment hesitation in which a delay or
tilting past their limits of stability and complete inability to initiate a step
Because bradykinesia is due to im- in response to external displace- occurs.76 Freezing not only slows
paired central neural drive, rehabili- ments associated with hitting or walking, but it also is a major con-
tation to reduce bradykinesia should punching a boxing bag. To reduce tributor to falls in people with PD.77
focus on teaching patients to in- bradykinesia, patients should be en- It is a poorly understood phenome-
crease the speed, amplitude, and couraged to “think big”42 while in- non that is associated with executive
temporal pacing of their self-initiated creasing the speed and amplitude of disorders in people with PD.76,78
and reactive limb and body center- large arm and leg movements Freezing during gait occurs more of-
of-mass (CoM) movements. Table 2 throughout agility courses and dur- ten when a person is negotiating a
presents representative exercises ing multidirectional lunges and box- crowded environment or narrow
aimed at reducing bradykinesia for ing (Tabs. 2 and 3). Walking sticks doorway, when making a turn, or
mobility. These exercises may pro- may help patients attend to the large, when attention is diverted by a sec-
mote weight-shift control and pos- symmetrical arm swing that is coor- ondary task.77,79 Jacobs and Horak80
tural adjustments in anticipation of dinated with strides during gait. recently found that freezing or “start
voluntary movements such as hesitation” in step initiation is asso-

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A Sensorimotor Agility Exercise Program for People With Parkinson Disease

Table 3.
Progressions for Each Activity

A. Kayaking: Kayaking focuses on counter-rotation of shoulder and pelvic girdle and axial trunk rotation.

Level Surface Vision Resistance Dual Task

1 Sit on a chair Normal, well-lit room Holding pole Counting

2 Sit on DynaDisca Sunglasses 3-lb pole Verbal: make a list

3 Stand on firm surface No-body glasses 6-lb pole Verbal/cognitive: math

B. Agility course: The agility course includes turns, doorways, hallways, and small areas. The tasks include high knees
walking with hands touching knees, skipping, lateral shuffles, grapevine, and tire course. Advanced individuals may add
agility on an inclined surface and bouncing or tossing a ball.

Arms and Trunk (High Knees


Level Speed/Agility Dual Task and Tire Course Only)

1 Self-paced Count steps out loud Self-selected

2 Increase speed Motor task: toss ball between hands Reciprocal arms

3 Quick changes in direction, pace, Cognitive task: math Add head and trunk rotation
stop and go

C. Boxing: The boxing task includes simple to complex combinations involving jabs, hooks, and crosses.

Level Plane of Movement Speed Dual Task

1 Lateral stance to the bag Self-paced Count punches

2 Pivot with back foot Bursts of speed: combo punches for 15 s Name punches (hook, jab, cross)

3 Walk backward around bag Bursts of speed: combo punches for 30 s Cognitive task while maintaining pattern

D. Lunges: Three types of lunges use these progressions: (1) lunges for postural correction, (2) clock stepping (multidirectional,
in-place) lunges, and (3) dynamic lunges during locomotion.

Arms and Trunk


(Dynamic
Level Surface External Cue Vision Resistance Dual Task Lunges Only)

1 Firm surface Rubber discs Well-lit room None None None


designate foot
placement

2 One foot on compliant Decrease disc size Sunglasses Weight vest (start Motor task: trunk Use arms
surface (DynaDisc/ or number with 10% of reciprocally
foam mat) body weight)

3 Foam mat (both feet) No discs No-body glasses Increase vest Verbal or cognitive Lift arms over head
weight, 5% of while holding
body weight ball
increments
a
DynaDisk manufactured by Exertools Inc, 320 Professional Center Dr, #100, Rohnert Park, CA 94928.

ciated with repetitive, anticipatory, affected by freezing, agility exercises or gym, where obstacle courses have
lateral weight shifts and that people should be performed in environ- been set up that require turning
who are healthy can be made to ments in which freezing typically oc- quickly, negotiating narrow and
“freeze” when they do not have time curs. As shown in Tables 2 and 3, tight spaces such as corners, ducking
to preplan which foot to use when exercises that involve high stepping, under and stepping over obstacles,
initiating a compensatory or volun- skipping, or taking large steps in dif- picking up objects while walking,
tary step. Therefore, freezing may ferent directions through doorways and quickly changing directions and
be related to difficulties in shifts of and over and around obstacles, such foot placement. Once a person suc-
attention, preplanning movement as between chairs placed shoulder- cessfully performs the agility exer-
strategies, or quickly selecting a cor- width apart, could potentially re- cises on an obstacle course, more-
rect central motor program. duce freezing episodes. Quick turns advanced progressions could be
should be practiced in corners and introduced, such as performing dual
To help people in the early stages of near walls. Individuals with PD could cognitive tasks while maintaining
PD reduce their chances of being perform these exercises in the home form and speed on agility tasks.

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A Sensorimotor Agility Exercise Program for People With Parkinson Disease

Inflexible Program Selection and tion of whole-body movements. In- seen. In addition, many of the exer-
Poor Sequential Coordination corporating boxing actions into a re- cises can be performed on a variety
Research suggests that the basal gan- membered sequence is another way of surfaces to require adaptation to
glia play an important role in task to practice the quick selection and altered somatosensory information
switching, motor program selection, sequencing of complex motor pro- from the surface. External feedback
and suppression of irrelevant infor- grams for mobility. To address prob- and sensory cues from the therapist
mation before executing an action.52 lems of quick program selection, regarding quality and size of the
The inability to quickly switch motor lunges and agility exercises also pro- movements should be used initially
programs has been demonstrated in vide practice changing motor strate- and progressively decreased as pa-
individuals with PD by an inability to gies during stopping, starting, chang- tients develop a more accurate inter-
change postural response synergies ing direction, changing stepping limb, nal sense of body position. As shown
in the first perturbation trial after a and changing the size and placement in Table 3, the sensorimotor agility
change in support, change in instruc- of steps. program used as an example in this
tions, or change in perturbation di- article progresses with traditional
rection.51,81 Dopamine replacement Sensory Integration progressive challenges95 (increasing
does not improve inflexible program There is strong evidence that the resistance, speed of gait, endurance,
selection.82,83 The difficulty with basal ganglia are critical for high- and so on) and with sensorimotor
switching motor programs manifests level integration of somatosensory challenges (dual tasking and changes
in difficulty maneuvering in new and and visual information necessary to in base of support, visual input, and
challenging environments and in form an internal representation of surface conditions).
changes in postural transitions, such the body and the environment.87,88
as turning, standing from a sitting Despite clinical examinations of pa- Cognitive Constraints
position, and rolling over.84 In addi- tients with PD revealing only incon- The inability to simultaneously carry
tion to difficulty switching motor sistent, subtle signs of abnormal sen- out a cognitive task and a balance or
programs, people with PD have dif- sory perception,89,90 an increasing walking task has been found to be a
ficulty sequencing motor ac- number of studies are showing ab- predictor of falls in elderly people.96
tions.65,85,86 Patients with PD show a normal kinesthesia and use of propri- It is even more difficult for a person
delay between their anticipatory oception in people with PD. For ex- with PD than age-matched elderly
postural adjustments and voluntary ample, Wright et al55 and Horak et people to perform multiple tasks,86
movements, such as rising onto al64 found that individuals with PD possibly because the basal ganglia
toes65 or a voluntary step.66 These have an impaired ability to detect the are responsible for allowing auto-
findings suggest that mobility in peo- rotation of a surface or the passive matic control of balance and gait and
ple with PD is constrained by poor rotation of the torso and that this for switching attention between
coordination among body parts and poor kinesthesia is worsened by tasks.52,86 Postural sway increases
between voluntary movements and levodopa medication. Individuals most in individuals with PD who
their associated postural adjust- with PD also show impaired percep- have a history of falls when a cogni-
ments, as well as by difficulty in tion of arm position and movement tive task is added to the task of quiet
switching motor programs appropri- and decreased response to muscle stance.97 These findings suggest that
ate for changes in task constraints. vibration.91–93 The poor use of pro- the ability to carry out a secondary
prioceptive information and de- cognitive or motor tasks while walk-
Consequently, an exercise program creased perception of movement are ing or balancing is a critical element
should include complex, multiseg- associated with over-estimation of of mobility that is a particular chal-
mental, whole-body movements and body motion (bradykinesia) and lenge in people with PD.
should include tasks requiring quick over-dependence on vision.50,94
selection and sequencing of motor An agility program could progress
programs such as practicing postural To facilitate use of proprioceptive task difficulty by adding cognitive or
transitions (eg, moving from stance information and reduce over- motor tasks that teach patients with
to the floor, rolling, and arising from reliance on vision, an agility program PD to maintain postural stability dur-
the floor to stance). As shown in should progress balancing and walk- ing performance of secondary tasks.
Table 2, one such exercise approach ing tasks by: (1) wearing dark sun- Table 3 presents exercises in which
is tai chi, which helps patients to glasses to reduce visual contrast sen- it is safe and appropriate to add a
learn increasingly complex se- sitivity and (2) use of “no body” dual cognitive or motor task. The
quences of movement and to focus glasses to obscure the bottom half of exercises at level 1 have no dual
on smooth timing and synchroniza- the visual field so the body cannot be tasks, level 2 has a motor task (eg,

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A Sensorimotor Agility Exercise Program for People With Parkinson Disease

bouncing a ball) added to the basic cervical rotation and speed, with posture and gait, the principles of
exercise such as an agility course, large, coordinated arm movements. neural plasticity, and the inevitable
and level 3 has a cognitive task (eg, Category III, “agility course,” focuses constraints of PD that ultimately af-
performing math or memory prob- on quickly changing motor programs fect dynamic balance and mobility.
lems) added to the same basic exer- such as quick turns, sequencing ac- These principles of the program in-
cise. The progression of adding sec- tions, and overcoming freezing. Cat- clude a focus on self-initiated move-
ondary tasks to gait and balance tasks egory IV, “boxing,” focuses on build- ments, big and quick movements,
serves as a training device as well as ing the patient’s agility and speed, large and flexible CoM control, re-
a tool to help patients understand the backward walking, and components ciprocal and coordinated move-
relationship between safe mobility of anticipatory and reactive postural ments of arms and legs, and rota-
and secondary tasks in everyday life. adjustments in response to a moving tional movements of torso over
bag. Category V, “lunges,” helps pa- pelvis and pelvis over legs. Flexible,
A Sensorimotor Agility tients with PD practice large CoM rotational axial motion of trunk and
Program for People movements, multidirectional limits of neck are stressed to achieve erect
With PD stability, and steps for postural correc- postural alignment, strengthening of
In this article, we propose a novel tion. Category VI, “pre-Pilates,” is a set extensors, and lengthening of flex-
sensorimotor agility program tar- of exercises that help patients with PD ors. Our program is designed to fa-
geted at constraints on mobility in extend and strengthen the spine, as cilitate sensory integration for bal-
people with PD. The expertise that well as practice postural transitions ance, emphasizing the use of
contributed to the program includes such as sit-to-stand maneuvers, floor somatosensory information to move
an internationally recognized neurol- transfers, and rolling.18 the body’s CoM quickly and effec-
ogist specializing in movement disor- tively for balance and mobility. Sec-
ders for more 35 years and 5 physical The sensorimotor progressions of ondary cognitive tasks are added to
therapists experienced in treating exercises II through V follow 3 levels mobility tasks to automatize control
people with PD, including 3 with of difficulty (Tab. 3). Progressions in- of balance and gait. This sensorimo-
PhDs with a focus on PD. Six certi- clude: (1) reducing the base of tor agility approach to mobility train-
fied athletic trainers who regularly support, (2) increasing surface com- ing is intended for prevention of mo-
work with people with PD also were pliance to reduce surface somato- bility disability but may be modified
helpful in designing the program. sensory information for postural ori- for patients at later stages of PD pro-
We propose that the exercise pro- entation, (3) increasing speed or gression to improve their mobility.
gram outlined in Table 2 could last resistance with weights, (4) adding
60 minutes, with about 10 minutes secondary cognitive tasks to auto- Both authors provided concept/idea/project
for each category of exercise. The mate posture and gait, and (5) limit- design, writing, and project management.
exercises in the 6 categories were ing visual input of the body with “no Dr Horak provided fund procurement, facil-
body” glasses or of the environment ities/equipment, institutional liaisons, and
selected to target one or more of the consultation (including review of manuscript
constraints on mobility (Tab. 1). with dark sunglasses to increase use
before submission).
of kinesthetic information. Category
I (tai chi) and category Vl (pre- The exercise program developed out of
Although not all people with PD brainstorming sessions with the following
have all of the constraints addressed Pilates) exercises progress by in-
expert neurologists, scientists, physical ther-
in this article, it may be that exercise creasing the length of remembered apists, and trainers: Fay B Horak, PT, PhD, Jay
should target all of these constraints, sequences and improving the form Nutt, MD, Laurie A King, PT, PhD, Sue Scott,
as each constraint generally is asso- of each subcomponent of the move- CT, Andrea Serdar, PT, CNS, Chad Swanson,
ments. All of these sensorimotor pro- CT, Valerie Kelly, PT, PhD, Ashley Scott, CT,
ciated with the progression of PD David Vecto, CT, Triana Nagel-Nelson, CT,
and eventually has a marked effect gressions were chosen specifically to
Kimberly Berg, CT, Nandini Deshpande, PT,
on mobility. Addressing constraints target the predictable constraints on PhD, and Cristiane Zampieri, PT, PhD. Straw-
early may delay the onset of related mobility due to PD, and testing of the berry Gatts, PhD, provided expert advice to
mobility deficits. Category I, “tai chi,” program is currently under way. select and modify tai chi moves for people
with Parkinson disease.
is a whole-body exercise that focuses
on developing a sense of body kines- Summary This work was supported by a grant from the
thesia, improving postural alignment, We present a progressive sensorimo- Kinetics Foundation and by a grant from the
tor agility exercise program for pre- National Institute on Aging (AG006457).
and sequencing of whole-body move-
ments that move the CoM. Category vention of mobility disability in peo- Dr Horak was a consultant for the Kinetics
II, “kayaking,” focuses on trunk and ple with PD. The program is based Foundation. This potential conflict of interest
on the role of the basal ganglia in

April 2009 Volume 89 Number 4 Physical Therapy f 391


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A Sensorimotor Agility Exercise Program for People With Parkinson Disease

has been reviewed and managed by Oregon 14 Herman T, Giladi N, Gruendlinger L, Haus- 30 Schmidt RA. Motor Control and Learning:
Health and Sciences University. dorff JM. Six weeks of intensive treadmill A Behavioral Emphasis. Champaign, IL:
training improves gait and quality of life in Human Kinetics Inc; 1982.
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study. Arch Phys Med Rehabil. 2007;
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to focal sensorimotor cortical damage. Exp
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April 2009 Volume 89 Number 4 Physical Therapy f 393


Downloaded from http://ptjournal.apta.org/ by Alan Daniel on March 11, 2015
Delaying Mobility Disability in People With Parkinson
Disease Using a Sensorimotor Agility Exercise
Program
Laurie A King and Fay B Horak
PHYS THER. 2009; 89:384-393.
Originally published online February 19, 2009
doi: 10.2522/ptj.20080214

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