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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.]

© 2009 American Physical Therapy
Association




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384   f     Physical Therapy   Volume 89    Number 4                                                                   April 2009
                                  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
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


386   f   Physical Therapy   Volume 89   Number 4                                                                    April 2009
                                         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-


April 2009                                                                                      Volume 89   Number 4        Physical Therapy f       387
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-


388     f    Physical Therapy       Volume 89     Number 4                                                                                      April 2009
                                                    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.


April 2009                                                                                                   Volume 89        Number 4      Physical Therapy f        389
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,


390   f   Physical Therapy   Volume 89   Number 4                                                                 April 2009
                                  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
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.
This article was received July 11, 2008, and            patients with Parkinson’s disease: a pilot       31 Chu CJ, Jones TA. Experience-dependent
                                                        study. Arch Phys Med Rehabil. 2007;
was accepted January 12, 2009.                          88:1154 –1158.                                      structural plasticity in cortex heterotopic
                                                                                                            to focal sensorimotor cortical damage. Exp
DOI: 10.2522/ptj.20080214                            15 van Eijkeren FJ, Reijmers RS, Kleinveld MJ,         Neurol. 2000;166:403– 414.
                                                        et al. Nordic walking improves mobility in       32 Isaacs KR, Anderson BJ, Alcantara AA, et al.
                                                        Parkinson’s disease. Mov Disord. 2008;              Exercise and the brain: angiogenesis in the
                                                        23:2239 –2243.
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392   f    Physical Therapy     Volume 89      Number 4                                                                                      April 2009
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