Sunteți pe pagina 1din 11

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 introcliiccM u new framework for therapists to develop an exereise
Oregon. program to delay mobilit)- 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, agilit}'. and flexihilit)-. all of which are affected by PI). This article summa-
junct Professor of Physiology and rizes recent research identify ing how constraints on mobility- specitic to PI), such as
Biomedicai 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 FI). Based on
Health and Sciences University, these constraints, a conceptual framework for exercises to maintain and improve
West Campus, Building 1, 505
mobility is presented. An example of a constraint-focused agility exercise program,
NW 185th Ave, Beaverton, OR
97006-3499 (USA). Address all incorporating movement principles from tai cbi, kayaking, boxing, lunges, agility
correspondence to Dr Horak at: training, and Pilâtes exercises, is presented. This new constraint-focused agilit)'
horakf@ohsu.edu. exercise program is based on a strong scientific framework and includes progressive
levels of sensorimotor, resistance, and coordination challenges that can be custom-
[King LA, Horak FB. Delaying mo-
bility disability in people with Par- ized for each patient while maintaining fidelity. Principles for improving mobilit>-
kinson disease using a sensorimo- pre.sented 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

Post a Rapid Response or


find The Bottom Line:
wvfw.ptjournal.org

384 Physical Therapy Volume 89 Number 4 April 2009


A Sensorimotor Agility Exercise Program for People With Parkinson Disease

that the basal ganglia are critical for Why Exercise May Prevent
M
ost people who are diag-
nosed with Parkinson dis- sensorimotor agility.^ Critical as- or Delay Mobility Disability
ease (PD) do not constüt pects of mobilit)- disability in people in People With PD
with a physical therapist until they with PD, sucb as postural instability, Exciting new findings in neuro-
already have obvious mobility prob- are unresponsive to pharmacological science regarding tbe effects of ex-
lems. However, it is possible that a and surgical therapies," 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 maintaitiing or improving their agil- neurological disorders. Specifically,
problems. Altbougb tbere are excel- ity to slow or reduce their decline in animal studies have demonstrated
lent guidelines for physical thera- mobilit}\ neurogenesis," an increase in dopa-
pists to treat patients with PD who mine syntliesis and release.'' and in-
exhibit mobility problems in order Tbis article uses the known sensori- creased dopamine in tbe striatum fol-
to improve or maintain their mobili- motor impairments of PD that affect lowing acute bouts of exercise.'"
ty, ' '^ there is little research on balance, gait, and postural transi- Such changes in tbe 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 w^itb PD. delay disability and maintain or im- brain to make new synaptic connec-
prove mobility' in people with PD. tions), neuroprotection, and slowing
The maior cause of disabilit>' in peo- This framework is based on the cur- of neural degeneration." '- Studies
ple witb HD is impaired mobility.^ rent knowledge of the neurophysi- with parkinsonian rats have sug-
Mobility, the ability of a person to ology of PD and the inevitable c(ïn- 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 b) changing brain function.
tional tasks.' requires dynamic neu- entilically based principles presented Specifically, rats that ran on a tread-
ral control to quickly and effectively here, which are focused on mobility mill sbowed preservation of dopami-
adapt locomotion, balance, and pos- disorders in people with PD. can be nergic cell bodies and terminals" '^
tural transitions to changing environ- incorporated into an existing ther- associated witb improved nmning
mental and task conditions. Such dy- apy program for people with PD. distance and speed,'- indicating a
namic control requires sensorimotor neuroprotective effect of exercise.
agility, wliich 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, tbe are currently testing in a clinical trial. loss of dopaminergic terminals. ' '
ability to quickly switcb motor pro- This program is unique in that it en- Aerobic exercise, sucb as treadmill
grams wben environmental condi- courages a partnership among phys- training and walking programs, bas
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.•^•'' 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,'''-'^However, it is not
with the progression of PD suggest dently in the communit). It is likely clear whether aerobic training, by
that a mobility program, sucb as the itself, is the best approach to improv-
one presented here, would need to ing inability, which depends upon
be sustained and modified through- dynamic balance, dual tasking, nego-
Available With out the course of the disease to main- tiating complex environments, quick
This Article at cbanges in movement direction, and
www.ptjournal.org tain maximal benefit.
other sensorimotor skills affected by
PD. It is possible that treadmill train-
• Audio Abstracts Podcast ing, for example, could be even
This article was published ahead of more effective for addressing com-
print on February 19, 2009, at plex mobility issues for people witb
www.ptiournal.org.

April 2009 Volume 89 Number 4 Physical Therapy 385


A Sensorimotor Agility Exercise Program for People With Parkinson Disease

PI) if the therapist could incoqîorate challenges into a comprehensive ex- Constraints Affecting
tasks such as dual tasking, balance ercise program directed at delaying Mobility in People With PD,
iralninii. and set-switching into a and reducing mobility problems in With Implications for the
ircadniill program. individuals with PD.
Sensorimotor Agility
liiere currently are many untested Reduce Mobility Program
exercise program.s availahic tor peo- Constraints With Exercise Rigidity
ple with PD'"-''' as well as several People with mild or newly diag- Parkinsonian rigidit>' is characterized
randomized controlled studies that nosed PD often do not have obvious by an increased resistance to passive
test specilic exercises, such as muscle weakness or poor balance. ^-^ movement thn)ugh(Hit the entire
strength (force-generating capacit>') Nevertheless, the literature suggests range of motion, in both agonist and
training or gait training.-"-"' llie ajv that muscle weakness, secondary- to antagonist muscle groups.'*'^°^~ The
proach presented in this article is abnormal muscle activation asstjci- functional outcomes ol rigidity, in
focused on exercises that challenge ated with brad\kinesia and rigidity, general, include a Hexed posture,"^^
sensorimotor control ot dynamic hal- can be present at all stages of lack of trunk rotation.'*'"''' and
ance and gait to improve mobilit) in PD."-'~ Similarly, balance and mo- reduced joint range of movement
people with PD. There are many bility problems ma)- be present in during postural transitions ant-l
other aspects of PD that also must be people with mild PD but only be- gait.'^*''^"' Electrom)(>graphy studies
addressed in rehabilitation. come apparent wben more-complex have shown that people with PD
coordination is required under chal- have high tonic background activity,
Drive Neuroplasticity lenging conditions. '**•''' For example, especially in the flexors, and co-
With Task-Specific mobility problems may only be ap- contraction of muscles during m()\ e-
parent when an individual with PD ment, especially in the axial mus-
Agility Exercise is attempting to walk quickly in a cles.'''"'^" In addition, antagonist
Studies in rats have demonstrated cluttered environment while talking muscle activation is larger and ear-
tliat task-specihc agility training (eg. on a cell phone. As the disease pro- lier, resulting in coactivation of mus-
acrobatic, environmental enricliiuent- gresses, balance problems become cle groups during automatic postural
type. high-beam balance course) re- more apparent, just as patients begin responses.*"'
sults in larger improvements in mo- to show impaired kinesthesia and
tor skills as well as larger changes in inability to quickly change postural Another characteristic of parkinso-
synaptic plasticity than simple, re- strategies.'^"'^' The basal ganglia af- nian rigidity is axial rigidity, which
petitive aerobic training sucli as run- fect balance and gait by contributing results in a loss of natural vertebral,
ning on treadmills.^" ''^ 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 Hexibility and range of motion
more effective than aerobic or gen- programs quickly, sequencing ac- that accompanies efficient postural
eral exercise to improve task peribr- tions, and using proprioceptive in- and locomotor activities.**"''-^ Wright
niance in patients with stroke.^'••^'' formation for kinesthesia and muiti- et aP'' found that rigidit)' in the neck,
Task-specific exercises targeted at a segmental coordinatitjn.''-''' 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, sensor)' inte- subjects when measuring the tor-
example, exercises targeted at im- gration, itillexible 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.- 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 rigidit)."^^ The high axial tone
satory stepping have individually bility, and the goals of exercises that (velocity-tlependent 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.
hiiity.'»-¿¿.38-42 We have borrowed utes to their characteristic 'en bloc"
singular techniques from .several suc- trunk motions, which make it difli-
cessful prognims and combined them cult for them to perform activities
with task-specific components of mo- .such as rolling over in bed or turning
bility and systematic sensorimotor while walking.''-

386 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 Constraints"

Constraints Impact on Mobility Exercise Principles

1. Rigidity Agonisl/antagonist co-contraction Trunk rotation


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

tl. 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. Infiexible 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 KInestbetic awareness


imbalance on unstable surface Decrease surface dependence
Poor alignment witb 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)

'CoM = centef of mass.

Scheiikman et al'"'' showed that ex- Bradykinesia responses in people with PD gener-
ercise can increase tnink flexibility Bradykinesia is most commonly de- ally are not improved by antiparkin-
in people with PD. We propose fined as slowness of voluntar>- move- sonian medicatiotis, highlighting the
an agility program that includes ment,^^ hut 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.'' Bradykinesia
aniagonist muscle co-contmction (ie, perturbations and atiticipatory pos- aLso is seen in postural transitions such
reciprocal movements), promote ax- tural adjustments. Reactive postural as turning"'" and the supine-tostand
ial rotation, lengthen the flexor mns- responses to surface translations''' ''^ manuever,^'' as well as in single-joint
clcs, and strengthen the extensor and anticipatory posturaJ movements movements"' ;md multi-joint reacliiog
muscles to promote an erect pos- prior to rising onto toes'*** and prior movements"- in people with PD.
ture. Rigidity can potentially be ad- to step initiation*'*' arc hradykinetic
dressed with kayaking, an exercise in patients with PD. Bradykinetic vol- Bnidy-kinesia is evident in slowed
in which the person counter-rotates untary stepping and postural com- rate of increase and decrease of mus-
tiie slioiilder and pelvic girdle; tai pensatory- stepping are characterized cle activation patterns.""* Reduction
chi, a set of exercises that focuses on hy a delayed time to lift the swing in muscle strength in people with PD
the individuals awareness of pos- liiiib, a w^eak push-off, reduced leg lift, has been attributed primarily to re-
tural alignment during postund tran- a small stride length, and lack of ami duced conical drive to muscles be-
sitions; and pre-Pilates, a series of swing,*'' »'-•<'•'<'"• Bradykinesia also is cause volutitary contraction, but not
exercises aimed at increasing spinal apparent in reduced voluntary and muscle response to nerve stimula-
mohility and lengthening flexor mtis- reactive limits of stability, especially tion, is weak in these intlividtials,"' ""^
cles groups. In addition, the program in the backward direction,"**'" The Electromyographic acti\it>- in bradyki-
shouid 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 btirsts and is not well scaled
sition to sitting on the floor and hack for bradykinetic anticipatory ixjstural for changes in movement distance or
again tliat emphasize trunk and head adjustments prior to a step, at the velcK'ity.^' Years of bradykinesia from
rotation (Tahs. 2 and 3)-'" expense of reduced lateral postural abnormal, centnilly driven muscle
stability'.*'" *''> Bnidykinetic postural control and abnormal, inefificient pat-

April 2009 Volume 89 Number 4 Physical Therapy • 387


A Sensorimotor Agility Exercise Program for People With Parkinson Disease

Table 2.
Representative Agility Exercise Program, With Progressions

Exercise Actions Progressions


1. Tai chi: Increase limits ot 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 whiie walking forward
Repulsing the monkey: deliberate slow, backward
walking, with diagonal weight shifts

IL Kayakirig: 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 )ab: short, straight punch from shoulder Speed, dual task, walking fonward, 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: tear» 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

Vl. 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 maj- 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 wliich a delay or
tilting past their limits of stability' and complete inability to initiate a step
Because bradykinesia is due io im- in response to external displace- occurs."'' 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 sbould punching a boxing bag. To reduce tributor to falls in people with PI).""
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"^-* 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."''""
and reactive limb and body center- large arm and leg mt)\'ement,s 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 lai^e, when attention is diverted by a sec-
mote weight-shift control and pos- symmetrical arm swing that is coor- ondan,' task."""''Jacobs and Horak""
tural adjustments in anticipation of dinated with strides during gait. recently found tbat freezing or "start
voluntary movements such as hesitation " in step initiation is asso-

388 Physical Therapy Volume 89 Number 4 April 2009


A Sensorimotor Agility Exercise Program for People Witii Parltinson Disease

Table 3.
Progressions for Each Activity
A. Kayaking: Kayakint) 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 DynaDisc" Sunglasses 3-lb pole Verbal: make a list

3 Stand on firm surface No-body glasses 6-ib pole Verbal/cognitive; math

B. Agility course: The agility course Includes turns, doorways, hallways, and tmali areas. The tasks Include high knees
walking with hands touching knees, skipping, iateral shuffles, grapevine, and tire course. Advanced individuals may add
agility on an Incilned surface and bouncing or tossing a bali.
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

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

C. Boxing: The hoxing task inciudes slmpie 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) iunges for posturai correction, (2) clock stepping (muitldirectionai,
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 No[ie 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

' DynaDisk manufactured by Exertools Inc, 320 Professional Center Dr, #100, Rohnert Park, CA 94928.

dated 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 comers, ducking
to preplan which foot to use when exercises that involve high stepping, under and stepping over obstacles,
initiating a compensator>' 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 he practiced in corners and introduced, such as performing dual
To help people in the early stages of near walls. Individuals with PI) could cognitive task.s while maintaining
PD reduce their chances of heing perform these exercises in the home form and speed on agility tasks.

April 2009 Volume 89 Number 4 Physical Therapy 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 imponant role in task to practice tbe 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 prol> and sensory cues from the therapist
mation before executing an action.'^- lems of quick program selection, regarding quality and size of the
The inability to quickly switch motor lunges and agility exercises also prt> movements should be used initially
programs has been demonstrated in vide practice changing motor strate- and progressively decreased as pa-
individuals with PD b) an inability to gies during stopping, starting, chang- tients develop a more accurate inter-
change postural response synergies ing direction, changing stepping limb, nal setise 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.^'"' Dopamine replacement Sensory Integration progressive challenges"'^ (increasing
does not improve inflexible program Tbere is strong evidence that the resistance, speed of gait, endurance.
selection.'*2"^ The difficulty with basal ganglia are critical for high- atid so on) and witb 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.*^"""
as turning, standing irom a sitting Despite clinical examinations of pa-
position, and rolling over.*^* In addi- Cognitive Constraints
tients with PD revealing only incon- The inability to simultaneously carry
tion to difficulty switching motor sistent, subtle signs of abnormal sen-
¡irograms. people with FD have dif- out a cognitive task and a balance or
sory perception,""'"' an increasing walking task has been found to be :i
ficulty sequencing motor ac- number of studies are showing ab-
tions.''^ ""'«*' Patients with PD show a predictor of falls in elderly people.'^'
normal kinesthesia and use of propri- It is even more difficult for a person
delay between their anticipator)' oception in people with PD. For ex-
postural adjustments and voluntary- witb PD tban age-matched elderly
ample. Wright et aP"* and Horak et people to perform multiple tasks,"'~
movements, such as rising onto al"^ found that individuals with PD
toes''** or a voluntary' step.*"'' These possibly because the basal ganglia
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
ple with PD is constrained by poor matic control of balance and gait and
rotation of the torso and tbat this for switching attention between
coordination among body parts and poor kinesthesia is worsened by
between voluntary' movements and tasks.'^-•"'^' Postural sway increases
levodopa medication. Individuals most in individuals with PD who
their associated postural adjust- with PD also show impaired percep-
ments, as well as by difficulty in have a history of falls when a cogni-
tion of arm position and movement tive task is added to the task of quiet
switching motor programs appropri- and decreased response to muscle
ate for changes in task constraints. stance."" These findings suggest that
vibration.'^'-'^^ The poor use of pro- the ability to carry out a secondary
prioceptive information and de- cognitive or motor tasks while walk-
creased perceptiiin of movement are ing or balancing is a critical element
Consequently, an exercise program associated witb over-estimation of
should include complex, multiseg- body motion (bradykinesia) and of mobility that is a particular chal-
mental. whole-body movements and over-dependence on vision.'^"'" lenge in people with PD.
should include tasks requiring quick
selection and sequencing of motor An agility program could progress
programs such as practicing postural To facilitate use of propdoceptive task difficulty by adding cognitive or
transitions (eg. moving from stance information and reduce over- mottjr tasks tbat teach patients with
to the floor, roiling, 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 5 presents exercises in wbich
is tai chi, wbich 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. Ibe
quences of movement and to focus glasses to obscure the bottom half of exercises at level 1 bave no dual
on smooth timing and synchroniza- the visualfieldso the body cannot be tasks, level 2 has a motor task (eg.

390 Physical Therapy VolurTie 89 Number 4 April 2009


A Sensorimotor Agility Exercise Program for People With Parkinson Disease

bouncing a ball) added to the basie 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 memor)' prob- ()n quickly changing motor programs fect dynamic balance and mobility.
lems) added to the same basic exer- sueh 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 tcM)I to help patients understand the backward walking, and components ciprocal and coordinated move-
relationship between safe mohilirj' of anticipator)' and reactive postural ments of arms and legs, and rota-
and secondar>' tasks in everyday life. adjustments in response to a moving tional movements of ton>o over
hag. Categor\' V. •'lunges," helps pa- pelvis and pelvis over legs. Flexible,
tients with PD practice large CoM rotational axial motion of trunk and
A Sensorimotor Agility neck are stressed to achieve erect
movements, mtiltidirectit)nal limits of
Program for People stability, and steps for postural correc-postural alignment, strengthening of
With PD tion. Category VI, pre-Pilates," is a setextensors, and lengthening of Ilex-
In this article, we propose a novel of exercises that help patients with PD ors. Our program is designed to fa-
sensorimotor agility program tar- extend and strengthen the spine, as cilitate sensory integration for bal-
geted at constraints on mobility in well as practice postural transitions ance, emphasizing the use of
people with PD. The expertise that such as sit-to-stand maneuvers, floor somatosensory information to move
contributed to the program includes transfers, and rolling.'** the body's CoM quickly and effec-
an internationally recognized neurol- tively for balance and mobility. Sec-
ogist specializing in movement disor- ondary cognitive tasks are added to
ders for more 3^ years and 5 physical The sensorimotor progressions of
mobility tasks to automatize control
therapists experienced in treating exercises II through V follow 3 levels
of balance and gait. This sensorimo-
people with PD, including 3 with of difficulty (Tab. 3)- Progressions in-
tor agility approach to mobility train-
PhDs with a focus on PD. Six certi- clude: (1) reducing the base of
ing is intended for prevention of m o
fied athletic trainers who regularly support. (2) increasing surface com-
bility disability^ but may be modified
work with people with PD also were pliance to reduce surface somato-
for patients at later stages of PD p r o
helpful in designing the program. sensor>' information for postural ori-
gression to improve their mobility.
We propose that the exercise pro- entation, (3) increasing speed or
gram outlined in Table 2 could last resistance with weights. (4) adding
60 minutes, with about 10 minvites secondary cognitive tasks to auto-
for each category of exercise. The mate posture and gait, and (5) limit- Both authors provided concept/idea/project
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-
selected to target one or more of the body ' glasses or of the environment ities/equipment, institutional liaisons, and
constraints on mobility' (Tab. 1). with dark sunglasses to increase use consultation {including reviev^f of manuscript
of kinesthetic information. Categor\' before submission),
I (tai chi) and category VI (pre- The exercise program developed out of
Although not all people witb PD Pilates) exercises progress by in- brainstorming sessions with the follovi/ing
have all ot the constraints addressed creasing the length of remembered expert neurologists, scientists, physical ther-
in this article, it may be that exercise sequences and improving the form apists, and trainers: Fay B Horak, PT, PhD, Jay
should target all of these constraints, of each subcomponent of the move- Nutt, MD, Laurie A King, PT, PhD, Sue Scott,
as each constraint generally is asso- 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 gressions were chosen spccificalh' to David Vecto, CT, Triana Nagel-Nelson, CT,
and eventually has a marked effect target the predictable constraints on Kimberly Berg, CT, Nandini Deshpande, PT,
on mohilit)'. Addressing constraints mobility- due to PD, and testing of the PhD, and Cristiane Zampieri, PT, PhD. Straw-
early may delay the onset of related program is currently under way. berry Gatts, PhD, provided expert advice to
mobility deficits. Category' I, tai chi," select and modify tai chi moves for people
with Parkinson disease.
is a wliole-body exercise that focuses
on developing a sense of body kines- Summary This work was supported by a grant from the
thesia, improving postunil 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-bod> 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 391


A Sensorimotor Agility Exercise Program for People With Parkinson Disease

has been reviewed and managed by Oregon 14 Herman T. Cliladi N, Gruendlingt-r 1.. Haiis- 30 Schmidt ^\-Motor Control and Learning:
Health and Sciences University. dorff JM. Six weeks of intensive treadmill A fíehatiorai I'.tnphasis. Champaign, IL:
training improves gait and quality of life in Human Kinetics Inc: 1982,
This article was received ¡uly 1 /, 2008, and patients with Parkinson's disease: a pilot
study. Arch Phys Med Rdxibii. 200"': 31 Chu Í;J, Jones TA. Experienccdependent
was accepted January 12, 2009. structural plasticity in conex hcterotopic
88ll'i4ll';8
to focal sensorimotor cortical damage, Exp
DOI: 10.2522/ptj.20080214 15 van Eijkeren EJ, Reijmers RS. KIcinveld MJ. Neuroi. 2000:166:403-414.
et al. !\'ordic walking improves mobility in
Parkinson's disease, ,1/i^i' Disord. 2(k)8: 32 Isaacs KR, Anderson lij, .\lcaiiiara AA. et al.
23:2239-2243. Exeai.se and the brain: angiogenesis in the
References aduli rat cerelx-Uum after vigonnis physical
1 Ktus S|[. Biotm HR. Hendriks CI. etal. 16 Mtihlack S, Welnic J, Woitalta D, Muller T. activitv and motor skill learning. J Cereb
Evitk'iice-hased analysis of physical ther- Exercise improves efficacy of levodopa in Biood' ¡lou.Metai). 1992:12:110-119.
apy in Parkinson's distase with rtcom- patients with Parkinson's disease. Mov
Disord. 20()7;22:427-430. 33 i^olcomhe S. Kramer AF. Fitness effects on
nicndalions lur practice and research. the cognitive function of older adtilts: a
Mor i:>isord. 2l)(r:22:451-460. 17 Cianci H, Parkinsons Disease: Fitness meta-analytic study. Psydioi Sei. 2003:
2 Morris MF. Movtmcnt disorders in people Courtts- 3rd ed. Miami. EL: National Par- 14:125-130.
with Parkinson disease: a model for phys- kinson Foundation: 20(Ki.
34 Black JE, Isaacs KR. .\nderson HJ, et al
ical tliL-rapy. I'i.iys Tljor. 2(KK);80:57H-'>97. 18 Argue .1. Patkirtsotts Disease and the Att Learning causes sTnaptogenesis, whereas
3 Wood BH, liiicloughlA. Howron A, Walker of Moving. Oakland, CA: New Harbinger motor activity causes angiogenesis, in cer-
RW. Incidence and prediction of falls in Publications: 2000, ebeliarcortex of adult rats, ProcNatlAcad
Parkinson's disease: a pn)specti\c multi- 19 /id D. Delity tite Disease: Exercise attd Sd VSA. 1990:87:5568-5572.
disciplinar)' study. J Netiroi Xeurostiri; i'atkitisotis Disease. Columbus. Oil: Co- 35 Anderson BJ, Alcantara AA. Grcenougli
Psychiatry. 20(12:72:721-~2S. lumbus Health Works Production: 2(H)7. Wr, Motorskill learning: changes in syn-
4 I'atla AE. Shuniway-tiook A. Dimensions of 20 Palmer SS, MonimtrJA. Webster 13D, et al, aptic organization of rbc rat cerebellar cor-
mobility: dclîning the complexity and dif- Exercise therapy lor Parkinson s disease. tex. Ni'titobioi Leant Metn. 1996:66:
ficulty associated with community mobil- Arch Phys Med Rei.nibii. I986;67: 221-229.
ity../.4^'/»^ Phys Ad. 199S:7:-'-l9. 741-745. 36 Sullivan KJ, Brown DA. Klassen T, et al.
5 Shumway-Cook A, Wooltacott M. Motor 21 C:omella CL, Stebbins GT, Bnn\n-Toms N. Effects of task-specific locomotor and
Control: Weory and i'racticai Appiica- Goetz CCi. Physical therapy and Parkin- strength training in adults who were am-
tioits. Haliimore. MD: Williams & Wilkins; son's disease: a controlled clinical trial, bulator> aficr stroke: resulls of the STEPS
I99S. Netitology. 1994:44(3 pt l):3~h-3"'H. randomized clinical trial. Pi.)ys Ther. 200"':
H~:]58O-l(iO2: discussion ÍW)3-I58T
6 Horak Fli, Macphearson .Ml, Postural ori- 22 Schenkman ,V1, Cutson IM, Kuchibhaila M.
entation and cquilihriuni. In: Rowfll Ul. et al. Exercise to improve spinal flexibility 37 Wolf SL. Winstein CJ, Miller JP. et al. Re-
Shepherd JR. eds. liattdhook of Physioi- and function for people with Parkinson s teniion of upper limb function in stroke
og): Section 12: lixerdse: Regulation and disease: a randomized controlled trial. survivors wbu have received constraint-
Integration of Midtipiv Systems. New J Atn Geriatr Soc. 1998;46:1207-1216. induced movement therapy: tbe FXC:n E
York, NY: Oxford University Press: 1996: randomi.sed trial. Lancet Neuroi. 2008:
2SS-292. 23 Hirsch MA, Toole T, Maitland C<;. Rider "':33- 40.
RA, The effects of balance iraining and
7 Bloem BR. van Viigc JP, Bcckley DJ. Pos- higb-intensity resistance training on per- 38 Morris M, Iansek R, Matyas TA, Summers
tur.ll instability and falls in Parkinson s dis- sons with idiopathic Parkinson's disease, JJ. Stride length regulation in Parkinson s
ease, Adv Neil roi 2001:87:209-223. Atch Phys Med Rehnbii. 200^:84: disease normalization strategies and un-
1109-1117. derlying mechanisms iirain. 1996:119:
8 van Praaji H. Kempt-nnann G. (iage FH, 551-568.
Ruiining increases cell proliferation and 24 Ellis T, de GtMfde CJ. Eeldman RG. ct al.
neuroyenesis in the adult mouse dentate Efficacy of physical tlierap) pn)grjm in 39 Viliani T, Pasqtietli P, Magnolfi S, ct al. Ef-
gyais. Ned Netiro.<!d 1999:2:26ii-2''O. patients with Parkinson's disease: a ran- fects of physical training on stniightening-
domized controlled trial. Arch Pijys Med up pnKesses in patients wiih Parkinson's
9 Heyes MP, (iamett ES, Coates Ci. Nigrostri- disease. Disahil RfhaiJtT. 1999:21:68-73.
atal dopaminergic activity is increased dur- Rehabii. 2005:86:626-632.
ing exhaustive exercise stress in rats. Life 25 Frutas Ej, Mitchell K, Williams A, et al. Gait 40 Mak MK. IIui-<;ban CW. Cued task-specific
Sei. I988;42:1'S37-H42. and step training to reduce falls in Parkin- training is better than exercise in improv-
son's disease, NeuroRehabilitatioti. 2005: ing sit-to-stand in ]>atients with Parkinson's
10 Meeiiscn R, De Meirleir K. Microdialysis as disease: a randomized controlled trial.
a method lo measure central cat- 20:1 «3-190.
Mor Disotd. 2(H)8:23:501-509.
echolamines during exercise. Med Sd 26 Burini I). Farabollini B. laciicci S. et al, A
Sports Exetc. 1994;26:S23- randomised controlled cross-over trial of 41 Jobges M. Heuschkei G. Pretzel C, et al.
aerobic training versus Qigong in ad- Repetitive training of compensator)- steps:
11 TillcrsonJI., Colien AD, Caudle WM, ci al. a therapeutic approach for postural insta-
Forced nonuse in unilatenü parkinsunian vanced Parkinson's disea.sf. Futa Medico-
/>hys. 2006;42:23l-238. bility in Parkinson sdisease.y jVi'/iio/Aie«-
rats exacerbates injiir>'. Neurosdence. rosurg Psychiatry. 2Ot)4:"'5:1682-1687.
2O«2;22:679O-6799. 27 Dibble LI-, Hale TE. Marcus RL, et al. Higli-
intensit;' resistance training amplifies mus- 42 Farley BG. Koshland GF, Iraining BIG to
12 Fisher BE, Pet/inger CiM, Nixon K, etal. move faster: tbe application of the speed-
Exercise-indticcd behavionil rt!co\'er\' and cle hypertrophy and functional gains in
persons with Parkinson's disease. Mov amplitude relation as a rehabiliiation strat-
neiiroplasticity in the l-methyl-4-phenyl- egy for people with Parkinson s disease.
I,2,.i,frtetralndropyddine-lesionfd mouse Disord. 2006:21:1444-1452.
Fxp Brain Res. 2()05:l67:-462-467.
basal ganglia. J Nearosci Res. 21MM ; 28 Schmiiz-Hubscli T. Pyfcr D. Kielwein K.
77:^78 .-39(i. et al. Qigong exercise for the symptoms of 43 Melnick M. Neurologic Rehabiiitation.
Parkinson's disease: a randomized, con- 3rd ed. St Uitiis. MO: Mosby: 1995.
13 Tiikrson jL. Caudle WM, Reveron ME,
Miller Ci'W. Exerci.sc induced behavioral trolled pilot study. Mov Disord. 2006: 44 Wierzbicka .MM, Wiegner AW, Logigian
recovery and attenuates ncurochemical 21:543-548. EL. Young KR. Abnormal most-rapid iso-
deficits in rodent models of Parkinson's dis- 29 Ashburn A. I-azakarley L, Ballinger C, et al. metric contractions in palienis with Par-
ease. Neurosdence. 2IM)3:119:899-911 A randomised controlled trial of a home kin.soii's disease._/ Neuroi Neurostirg Psy-
based exercise programme to reduce tbe chiatry 1991:54:210-216,
risk of falling among people with Parkin- 45 Stelmach tiE, Teasdale N, Phillips J, Wor-
son's disease, y .Setiroi Neurosnrg Psychi- ringham CJ, Force production characteris-
atry. 200"';-'8:6^8-6K-t, tics in Parkinson s disease. Fxp Iirain Rvs.
1989:''6:I65-172.

392 • Physical Therapy Volume 89 Number 4 Aprii 2009


A Sensorimotor Agility Exercise Program for People With Parkinson Disease

46 Coreos DM. Chen CM. Qtiinn NP. ct al. 62 Vaugoyeau M. Viailet V. Aurenty R. et al. Ax- 80 Jacobs _rv\ Honik FB. External posttiral per-
Strength in Parkinson's disease: relation- ial rotation in Parkinson's disease. / Neurol turbations indtice nitiltiple anticipator)'
ship to rjte ol force generation and clini- Neurosurg Psychiatry. 2(MKi;-^:8t5-821. posttiral adjustments when subjects can-
cal status. Ann Seurol l996;39;79-88. not pre-.select tbeir stepping fooi. Exp
63 Schenkman ML. c;utson TM. Kuebihbatla Brain Res. 2007; 179:29-42.
47 Inkster LM. EngJJ, Maclntjre DL, StoessI M, et al. Exercise to improve spinal llexi-
AJ. U'g mtiscle strength is reduced in Par- bility and function for people witb Parkin- 81 Chong RKY, Jones CL. Horak FB. Postural
kinson's disease and relates to tht- abilit>' son's disease: a randomized, controlled tri- set for balance control is normal in rUzliei-
to rise from a chair Mov Disord. 2003: al../M»; GeriatrSoc. 1998;46;1207-1216. mer's hut not in Parkinson's Disease. J
lH:l'i^-lC)2. Geronloi A Biol Sei med Sei. 1999:54:
64 Horak FH. Dimitrova D. Nutt JG. Direction- Ml 29-M 135.
48 Carpinclia I. Crenna V. Calabrese E, et al. specilic postural instabilité' in subjects
Locomutor function in the early stage of witb Parkinson's disease. Exp Neiiroi. 82 Tunik E, Feldman AG. Poizner H. Dopa-
Parkinson's disease. IEEE Trans Xeiinii 2005:193:504-521. mine replacement therapy does not re-
Syst RebaiJii Eng. 2(tO'';l'i:S43-551. store the ability of Parkinsonian patients to
65 Frank JS, Horuk FB. Nutt JCi. Centrally ini- make rapid adjii.stments in minor strate-
49 Rochester L. Hetherington V.Jones D, et a!. tiated pijsttirat adjustments in parkinso- gies according to changing sensorimotor
Attending to the task; interterence effects of nian patients on and off levodopa. y ,\eu- contexts. Parkinsonism Relat Disord.
ftinctional tasks on w:ilkijig in Parkinson's rophysiol 2OO0:84;244O-2448. 2007:15:425-433.
di.se;Lse and ilie R)les of cognition, depres-
sion, fatigue, and balance. Arch Phys Mvd 66 Burleigh-Jacobs A, Homk FB. Nutt J<;. 83 Horak FB. Ntitt jG. Nashner LM. Postural
Rehahii 2(HM;8S: 15- Obe.so JA. Step initiation in Parkinson's inllexibility in parkinsonian subjects.
disease; influence of levodopa and exter- / Seurol Sei. 1992:1 U:46-5H.
50 Maschke M. iiomcz CM, Tuite Pj, Konczak nal sensory triggers. .Mov Disord 199"';
J. Dysfunction of the basal ganglia, but not 12;206-2r';. 84 Steiger MJ, Thompson PD, Marsden CD.
the cerebellum, impairs kinaesthesia. Disordered axial movement in Parkinson's
Brain. 2OO.S;126<pt 10):23l2-2322. 67 Eüng 1J\, Horak FB. I-ueral stepping for disease. / .\enrol ,\eurosuri> Psychiatiy.
postural correction in Parkinson's disease. 1996;61;645-64«.
51 Chong RK. Horak f-B. Woollncott MH. Par- Arch Phys Med Reimbii. 2008;89:
kinson's disease impairs the ability to 492-499. 85 Brown RG. Marsden CD. Dual-task perfor-
change set quickly. J Neurol Scl. 2000; mance and processing resources in normal
175:57-70. 68 Maneini M. Roccbi L. Horak FB, Cbiari L. subjects and patients with Parkin.son's dis-
Effects of Parkinson's disease and levodopa
52 Yehene E, Meinm N, Sorokcr N. Basal gan- on functional limits of stability. Ciin Bio- ease, fím/í). 199I;ll4Cpt 1A);215-23I.
glia play a unique role in task switching mech (Bristol. Avon). 2(K)8;23:45O-458. 86 Hloem BR, Grimbergen YA, van Dljk JG,
within the frontnl-stibconical circuits; evi- Mtmnekc M. 'Ilie "[M)sture second" stniteg)':
69 Rocchi 1.. C;hiari L. Maneini M. et al. Step a review of wrong priorities in Parkinson's
dence from patients with focal lesions. / initiation in Parkinson's disease; infltience
Cogn .\eurosci. 2008; 20;1079-109i. distase.,/ Neurol Sei. 2(K)ÍÍ;2I8: l%-204.
of initial stanee conditions. Neurosci L.et.
53 Taniwaki 1. Ok;nania A. ^'osliiura T, et al. 2(t06;406;128-132. 87 DeLong MR. The neun)physiologic basis
Reappraisal of the motor role of basal of abnormal movement in basal ganglia
ganglia; a ñ.inctional magnetic resonance im- 70 Mak MK. Patia A, Htii-Cban C. Sudden turn disorders. Nei/rohchav Toxicol Teralol.
age stiidy.y.Vt'/ííYwo'. 2003;23;3432-3438. during walking is impaired in people with Í983;5;81I-816.
Parkinson s disease. Exp Brain Res. 2(HI8:
54 Í5n)wn P. Marsden CD What do the basal 190;43-51. 88 Lidsky T. Manetto C, Schneider J. A con-
ganglia do? Lancet. 1998;351(9118): siderjtii)n of sensory* factors involved in
71 Pfann KD. (kichman AS. Comella C;L, Cor- motor functions of the basal ganglia.
1S01-1H04. eos DM. Control of mo\ement di.stance in Brain Res. 1985;356;l33-i46.
55 Wright WG. Ciurñnkel VS, Nutt J(i, et al. Parkinson's disease. Mav Disord. 2001; 16;
Axial hypertonicit) in Parkinson's disease: 1048-1065. 89 Snider SR. Isgreen WP. Cote I,L Primary
direct measurements of trunk and hip sensoq* systems in Parkinsonism. Neurol-
torque. Exp Neuroi. 2()07;208;38-46- 72 Farley BG. Sherman S, Koshland GF. Sbotil- ogy. 1976;26;423-429.
der mtisele activity in Parkinson s disease
56 Hurleigh A, Horak 1-B, Nutt JCi, Frank JS during multijoint arm movements across a 90 Diamond SG. Schneider JS. Markham CH.
Levodopa reduces muscle tone and lower range of speeds. E.y/} Brain Re.s. 2004; Oral sensorimotor defects in patients with
extremity tremor in Parkinson's disease. 154:160-1-5. Parkinson s disease. Aäv Neurol. 1986;45:
Can J Netiroi Sei. iy95;22:280-285. 335-338.
73 Glendinning DS, Enoka RM. Motor unit be-
57 Mak MK. Wong Et:, Hui-Chan CW. Quan- havior in Parkinson's disease. Phys Wer. 91 Jobst BE. Melnick ME. Byl NN, et al. Sen-
titative measurement of trunk rigidit> in 1994:74:61-70. sor^' perception in Parkinson's disease.
parkinsunian puiems. J Neurol. 2OO7;254; Arch Seuroi. l997;S4;4S0-454.
74 Saleniiis S, Avikainen S, Kaakkola S. et at.
202-209. Defective cortical drive to muscles in Par- 92 Zia S. C«KJy FWJ. Olioyle DJ. Disturliance ol
58 Jacobs .I\'. Dimitrova DM. Nutt JC. Horak kinson's disease and its improvements human joint position sense in l*-.trkinson's
l"li. ('an stooped posture explain multidi- with Ic-vadopa. Brain. 2OO2:12'i;491-5OO. disease../ /*VSÍVÍ/. 199"*;5O4;1 17-118,
rectional postural instability in patients
with Parkinson's disease? Lixp Brain Res. 75 't anagawa S. Sliindo M, ^ anagisawa N. Mus- 93 Zia S. Cody FWJ, O'Hoyle DJ. Inipairmenl
2005;K)i):78-88. cidar Weakness in Parkinsons Disease. of discrimination of bilateral differences in
Vol. 53. NewYork, NY: Raven Press; 1990. the loci of tactile stimuli in Parkinson's
59 Schenkman ML, M<)re\- M. Kuehibliatia M. disease,,/ Physiol 1998;50y;l8(l-l8l.
Spinal tlexibilit)- and balance control among 76 Giladi N. Kao R, Fahn S. Freezing phenom-
enon in patients with parkinsonian syn- 94 Klockgether 1". Bonitta M. Rapp H, ft al. A
commiuiity-dwelling adtilts witli ;md with- dromes. Mov Disord. iy97:12;3O2-3O5. defect of kinesthesia in Parkinson's dis-
out Parkinson's disease. J derontoi A Biol
Sei Med Sei. 2(«H):55:M441-M445- 77 Bloem BR, Hausdorff JM, Visser JE, Giladi ease. Mov Disord. l99'>:10;460-465.
N. Falls and freezing of gait in Parkinson's 95 O'SulIivan SR, Schmitz TJ. Physicai Reha-
60 Sthenkman ML. Clark K. Xie T. et al. Spi- disease; a review of two interconnected, hii itat ion: .Assessment and Treatment.
nal movement and peri'ormance of a stand- episodic phenomena. Mov Disord. 2004; Piiiladelphia; FA Davis Company: 1994.
ing reach task in participants with and 19:871-884.
without Parkinson disease. Phys Tljer. 96 Lundin-OIsson L, Nyberg L, Gustafson Y.
2OO1:81;14OO-I4II. 78 Giladi N. McDermott MP. Fahn S. et al. "Stops walking when talking" as a predic-
Freezing of gait in PD; prospective assess- tor of falls in elderly people. Lancet.
61 Dimitrova D. Horak FR, Nutt JCi. Postural ment in the DATATOP cohort. Neurology. 1997:349(9052);61'".
mtiscie responses to multidirectional 2001;56:1712-1721.
tnmslations in patients with Parkinson's 97 Márchese R, Bove M, Abbruzzese G. Effect
disease../ Neurophysioi 2OO4;9I:489-5O1. 79 Giladi N, Hausdorff J.M. Tlie role of mental of cognitive and motor tasks on postural
function in the patbogenesis of freezing of stability in Parkinson s disease; a posturo-
gait in Parkinson s disease. J Neurol Sei. grapbic- study. Mov Disord. 2003:18;652-
2006;248:173-176. 658.

April 2009 Volume 89 Number 4 Pbysical Tberapy 393

S-ar putea să vă placă și