LA King, PT, PhD, is Post-doctoralFellow, Oregon Health andSciences University, Portland,Oregon.

FB Horak, PT, PhD, is ResearchProfessor of Neurology and Ad-junct Professor of Physiology andBiomedicai Engineering, Depart-ment of Neurology, OregonHealth and Sciences University,West Campus, Building 1, 505NW 185th Ave, Beaverton, OR97006-3499 (USA). Address allcorrespondence to Dr Horak at:horakf@ohsu.edu.

[King LA, Horak FB. Delaying mo-bility disability in people with Par-kinson disease using a sensorimo-tor agility exercise program. PhysTher. 2009;89:384-393.]

© 2009 American Physical TherapyAssociation

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Delaying Mobility Disability in PeopleWith Parkinson Disease Using aSensorimotor Agility Exercise ProgramLaurie A King, Fay B Horak

This article introcliiccM u new framework for therapists to develop an exereiseprogram to delay mobilit)- disability in people with Parkinson disease <PD). Mobility,or the ability to efficiently navigate and function in a variety of environments, requiresbalance, agilit}'. and flexihilit)-. all of which are affected by PI). This article summa-rizes recent research identify ing how constraints on mobility- specitic to PI), such asrigidity, bradykinesia, freezing, poor sensory integration, inflexible program selec-tion, and impaired cognitive processing, limit mobility in people with FI). Based onthese constraints, a conceptual framework for exercises to maintain and improvemobility is presented. An example of a constraint-focused agility exercise program,incorporating movement principles from tai cbi, kayaking, boxing, lunges, agilitytraining, and Pilâtes exercises, is presented. This new constraint-focused agilit)'exercise program is based on a strong scientific framework and includes progressivelevels of sensorimotor, resistance, and coordination challenges that can be custom-ized for each patient while maintaining fidelity. Principles for improving mobilit>-pre.sented here can be incorporated into an ongoing or long-term exercise programfor people with PD.

384 Physical Therapy Volume 89 Number 4 April 2009

A Sensorimotor Agility Exercise Program for People With Parkinson Disease

Most people who are diag-nosed with Parkinson dis-ease (PD) do not constüt

with a physical therapist until theyalready have obvious mobility prob-lems. However, it is possible that arigorous exercise program that fo-cuses on anticipated problems,which are inevitable with progres-sion of the disease, may help patientswho do not yet exhibit mobilityproblems. Altbougb tbere are excel-lent guidelines for physical thera-pists to treat patients with PD whoexhibit mobility problems in orderto improve or maintain their mobili-ty, ' ' there is little research onwhether exercise may delay or re-duce the eventual mobility disabilityin patients diagnosed w itb PD.

The maior cause of disabilit>' in peo-ple witb HD is impaired mobility.Mobility, the ability of a person tomove safely in a variety of environ-ments in order to accomplish func-tional tasks.' requires dynamic neu-ral control to quickly and effectivelyadapt locomotion, balance, and pos-tural transitions to changing environ-mental and task conditions. Such dy-namic control requires sensorimotoragility, wliich involves coordinationof complex sequences of move-ments, ongoing evaluation of envi-ronmental cues and contexts, tbeability to quickly switcb motor pro-grams wben environmental condi-tions change, and the ability to main-tain safe mobility during multiplemotor and cognitive tasks.• •'' Thetypes of mobility deficits inevitablewith the progression of PD suggest

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that the basal ganglia are critical forsensorimotor agility. Critical as-pects of mobilit)- disability in peoplewith PD, sucb as postural instability,are unresponsive to pharmacologicaland surgical therapies," making pre-ventative exercise an attractive op-tion. As yet, there is no known on-going exercise program for peoplediagnosed with PD that focuses onmaintaitiing or improving their agil-ity to slow or reduce their decline inmobilit}\

Tbis article uses the known sensori-motor impairments of PD that affectbalance, gait, and postural transi-tions to develop a conceptual frame-work to design exercises that aim todelay disability and maintain or im-prove mobility' in people with PD.This framework is based on the cur-rent knowledge of the neurophysi-ology of PD and the inevitable c(ïn-straints on mobility resulting frombasal ganglia degeneration. The sci-entilically based principles presentedhere, which are focused on mobilitydisorders in people with PD. can beincorporated into an existing ther-apy program for people with PD.

Based on this framework, this articlealso presents an example of a novelsensorimotor agility program that weare currently testing in a clinical trial.This program is unique in that it en-courages a partnership among phys-ical therapists, exercise trainers, andpatients to set up, progress, and re-evaluate an exercise program that ul-timately can be carried out indepen-dently in the communit). It is likelythat a mobility program, sucb as theone presented here, would need tobe sustained and modified through-out the course of the disease to main-tain maximal benefit.

Why Exercise May Preventor Delay Mobility Disabilityin People With PDExciting new findings in neuro-science regarding tbe effects of ex-ercise on neural plasticity and neu-roprotection of the brain againstneural degeneration suggest that anintense exercise program can im-prove brain function in patients withneurological disorders. Specifically,animal studies have demonstratedneurogenesis," an increase in dopa-mine syntliesis and release.'' and in-creased dopamine in tbe striatum fol-lowing acute bouts of exercise.'"Such changes in tbe brain may affectbehavioral recovery' as a result ofneuroplasticity (the ability of thebrain to make new synaptic connec-tions), neuroprotection, and slowingof neural degeneration." '- Studieswith parkinsonian rats have sug-gested that chronic exercise mayhelp reverse motor deficits in ani-mals b) changing brain function.Specifically, rats that ran on a tread-mill sbowed preservation of dopami-nergic cell bodies and terminals" 'associated witb improved nmningdistance and speed,'- indicating aneuroprotective effect of exercise.Conversely, nonuse of a limb in-duced by casting in parkinsonian ratsincreased motor deficits as well asloss of dopaminergic terminals. ' 'Aerobic exercise, sucb as treadmilltraining and walking programs, basbeen tested in individuals with PDand has been shown to improve gaitparameters, quality of life, and leva-dopa efficacy,'''-'^However, it is notclear whether aerobic training, byitself, is the best approach to improv-ing inability, which depends upondynamic balance, dual tasking, nego-tiating complex environments, quickcbanges in movement direction, andother sensorimotor skills affected byPD. It is possible that treadmill train-ing, for example, could be evenmore effective for addressing com-plex mobility issues for people witb

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A Sensorimotor Agility Exercise Program for People With Parkinson Disease

PI) if the therapist could incoqîoratetasks such as dual tasking, balanceiralninii. and set-switching into aircadniill program.

liiere currently are many untestedexercise program.s availahic tor peo-ple with PD'"-''' as well as severalrandomized controlled studies thattest specilic exercises, such asstrength (force-generating capacit>')training or gait training.-"-"' l l ie ajvproach presented in this article isfocused on exercises that challengesensorimotor control ot dynamic hal-ance and gait to improve mobilit) inpeople with PD. There are manyother aspects of PD that also must beaddressed in rehabilitation.

Drive NeuroplasticityWith Task-SpecificAgility ExerciseStudies in rats have demonstratedtliat task-specihc agility training (eg.acrobatic, environmental enricliiuent-type. high-beam balance course) re-sults in larger improvements in mo-tor skills as well as larger changes insynaptic plasticity than simple, re-petitive aerobic training sucli as run-ning on treadmills.^" ''' Task-specificexercise also has been shown to bemore effective than aerobic or gen-eral exercise to improve task peribr-niance in patients with stroke.^'••^''Task-specific exercises targeted at asingle, specific balance or gait im-pairment in patients with PD havebeen shown to be effective. Forexample, exercises targeted at im-proving small step size, poor axialmobility, difficulty with posturaltransitions, small movement ampli-tude, or slow speed of compen-satory stepping have individuallybeen shown to be effective in im-proving each particular aspect of mo-hiiity.'»-¿¿.38-42 We have borrowedsingular techniques from .several suc-cessful prognims and combined themwith task-specific components of mo-bility and systematic sensorimotor

challenges into a comprehensive ex-ercise program directed at delayingand reducing mobility problems inindividuals with PD.

Reduce MobilityConstraints With ExercisePeople with mild or newly diag-nosed PD often do not have obviousmuscle weakness or poor balance. -Nevertheless, the literature suggeststhat muscle weakness, secondary- toabnormal muscle activation asstjci-ated with brad\kinesia and rigidity,can be present at all stages ofPD."-'~ Similarly, balance and mo-bility problems ma)- be present inpeople with mild PD but only be-come apparent wben more-complexcoordination is required under chal-lenging conditions. '**•''' For example,mobility problems may only be ap-parent when an individual with PDis attempting to walk quickly in acluttered environment while talkingon a cell phone. As the disease pro-gresses, balance problems becomemore apparent, just as patients beginto show impaired kinesthesia andinability to quickly change posturalstrategies.'^"'^' The basal ganglia af-fect balance and gait by contributingto automaticity, self-initiated gait andpostural transitions, changing motorprograms quickly, sequencing ac-tions, and using proprioceptive in-formation for kinesthesia and muiti-segmental coordinatitjn.''-''' Duringthe progression of PD, mobility isprogressively constrained by rigidity,bradykinesia, freezing, sensor)' inte-gration, itillexible motor programselection, and attention and cogni-tion.- Table 1 summarizes con-straints on mobility due to PD, theImpact of these constraints on mo-bility, and the goals of exercises thatcould potentially reduce the impactof each constraint.

Constraints AffectingMobility in People With PD,With Implications for theSensorimotor AgilityProgramRigidityParkinsonian rigidit>' is characterizedby an increased resistance to passivemovement thn)ugh(Hit the entirerange of motion, in both agonist andantagonist muscle groups.'*' °^~ Thefunctional outcomes ol rigidity, ingeneral, include a Hexed posture,"^^lack of trunk rotation.'*'"''' andreduced joint range of movementduring postural transitions ant-lgait.' *'' "' Electrom)(>graphy studieshave shown that people with PDhave high tonic background activity,especially in the flexors, and co-contraction of muscles during m()\ e-ment, especially in the axial mus-cles.'''"'^" In addition, antagonistmuscle activation is larger and ear-lier, resulting in coactivation of mus-cle groups during automatic posturalresponses.*"'

Another characteristic of parkinso-nian rigidity is axial rigidity, whichresults in a loss of natural vertebral,pelvis/shoulder girdle, and femur/pelvis Hexibility and range of motionthat accompanies efficient posturaland locomotor activities.**"''-^ Wrightet aP'' found that rigidit)' in the neck,torso, and hips of standing subjectswas 3 to 5 times greater in subjectswith PD than in age-matched controlsubjects when measuring the tor-sional resistance to passive move-ment along the longitudinal axis dur-ing twisting movements. Levodopamedication did not improve theiraxial rigidit)."^^ The high axial tone(velocity-tlependent resistance tostretch) in patients with PD contrib-utes to their characteristic 'en bloc"trunk motions, which make it difli-cult for them to perform activities.such as rolling over in bed or turningwhile 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

1. Rigidity

tl. Bradykinesia

III. Freezing

IV. Infiexible program selection(sequential coordination)

V. Impaired sensory integration

VI. Reduced executive functionand attention

Impact on Mobility

Agonisl/antagonist co-contractionFlexed alignment of trunkReduced trunk rotationReduced ¡oint range of movementHigh axial tone (stiffness)

Slow, small movementsNarrow base of supportLack of arm swing

Poor anticipatory postural adjustmentsAbnormal mapping of body and movementAbnormal visual-spatial mapsDivided attention affects mobility

Poor rolling, sit-to-stand maneuvers, turnsDifficult floor transfersInability to change strategy quickly

Inaccurate without visionimbalance on unstable surfacePoor alignment witb environment

Difficulty with dual tasks and sequences of actions

Exercise Principles

Trunk rotationReciprocal movementsRhythmic movementsErect alignmentLarge CoM movementsIncrease limits of stability

Fast, large stepsCoM controlLarge arm swings

Improve weight shiftingUnderstand role of external cuesExercise in small spacesPractice dual tasks

Plan task in advanceQuick change strategiesSequencing components of task

KInestbetic awarenessDecrease surface dependenceFlexible orientation

Practice gait and balance with secondarytask and sequences of actions (ie; boxing,agility course)

'CoM = centef of mass.

Scheiikman et al'"'' showed that ex-ercise can increase tnink flexibilityin people with PD. We proposean agility program that includesmovements that minimize agonist-aniagonist muscle co-contmction (ie,reciprocal movements), promote ax-ial rotation, lengthen the flexor mns-clcs, and strengthen the extensormuscles to promote an erect pos-ture. Rigidity can potentially be ad-dressed with kayaking, an exercisein which the person counter-rotatestiie slioiilder and pelvic girdle; taichi, a set of exercises that focuses onthe individuals awareness of pos-tural alignment during postund tran-sitions; and pre-Pilates, a series ofexercises aimed at increasing spinalmohility and lengthening flexor mtis-cles groups. In addition, the programshouid include strategies for turningand transitioning from a standing po-sition to sitting on the floor and hackagain tliat emphasize trunk and headrotation (Tahs. 2 and 3)-'"

BradykinesiaBradykinesia is most commonly de-fined as slowness of voluntar>- move-ment,^^ hut it also is associated withslow and weak postural responses toperturbations and atiticipatory pos-tural adjustments. Reactive posturalresponses to surface translations''' ''and anticipatory posturaJ movementsprior to rising onto toes'*** and priorto step initiation*'*' arc hradykineticin patients with PD. Bradykinetic vol-untary stepping and postural com-pensatory- stepping are characterizedhy a delayed time to lift the swingliiiib, a w eak push-off, reduced leg lift,a small stride length, and lack of amiswing,*'' »'-•<'•'<'"• Bradykinesia also isapparent in reduced voluntary andreactive limits of stability, especiallyin the backward direction,"**'" Thecharacteristic narrow stance of pa-tients with PD may be compensatoryfor bradykinetic anticipatory ixjsturaladjustments prior to a step, at theexpense of reduced lateral posturalstability'.*'" *''> Bnidykinetic postural

responses in people with PD gener-ally are not improved by antiparkin-sonian medicatiotis, highlighting theneed for an exercise approach to thisconstraint on mobility.'' BradykinesiaaLso is seen in postural transitions suchas turning"'" and the supine-tostandmanuever,^'' as well as in single-jointmovements"' ;md multi-joint reacliiogmovements"- in people with PD.

Bnidy-kinesia is evident in slowedrate of increase and decrease of mus-cle activation patterns.""* Reductionin muscle strength in people with PDhas been attributed primarily to re-duced conical drive to muscles be-cause volutitary contraction, but notmuscle response to nerve stimula-tion, is weak in these intlividtials,"' ""Electromyographic acti\it>- in bradyki-netic muscles often is fractionated intomultiple btirsts and is not well scaledfor changes in movement distance orvelcK'ity. ' Years of bradykinesia fromabnormal, centnilly driven musclecontrol 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

1. Tai chi: Increase limits ot stability,improve perception of posture andcoordination of arms and legs andbackward and lateral large steps

IL Kayakirig: Trunk rotation,segmental coordination, speed

III. Agility course: Agility,multisegmental coordination, quickchanges in direction, and mobilityin tight spaces

IV. Boxing: Anticipatory posturaladjustments, postural corrections,fast arm and foot motions,backward walking, timing,sequencing actions

V. Lunges: Big steps, stepping forpostural correction, limits ofstability, quick changes indirection, internal representation ofbody

Vl. Pre-Pilates: Improve trunk control,axial rotation and extension,functional transitions, sequencingactions

Actions

Prayer wheel: anterior posterior slow, rhythmicalweight shifts coordinated with large arm circles

Cat walk; slow and purposeful steps, withdiagonal weight shifts

Cloud hands: slow lateral steps, with trunk verticalPart the wild horse's mane: coordination of arms

and legs whiie walking forwardRepulsing the monkey: deliberate slow, backward

walking, with diagonal weight shifts

Kayaking stroke: diagonal trunk rotation, withreciprocal forward arm extension and backwardarm retraction

High knees: high-amplitude stepping, with handslapping knees

Lateral shuffle: quick, lateral stepsTire course: wide-based, quick and high steps, with

turnsGrapevine cross: over coordinated steps

)ab: short, straight punch from shoulderCross: power punch, with trunk rotation, leading

arm crosses midlineHook: short, lateral punch, with elbow bent and

wrist twisted inward, trunk rotationCombinations: 2 or more punches delivered quickly

after one another

Postural correction: tear» until center of mass isoutside base of support, requiring a step; alldirections

Single multidirectional steps (clock stepping)Dynamic multidirectional lunge walking

Cervical range of motion, sit-to-stand maneuverFloor transfer, supine (bridging)Rolling (prone lying, progress to spinal extension

exercises)Quadruped (bird-dog, cat-camel, thread the

needle)Half-kneeling to stand

Progressions

Learn one action per week, starting withweight shifting and leg placement andprogressing to coordinated arm, neck,and torso motion

Speed, surface, resistance, vision, dual task

Speed, dual task, quick change in directions,tight and cluttered spaces, vision

Speed, dual task, walking fonward, walkingbackward, turns, remembered sequencesof action

Surface (up and down stool), external cues,vision, resistance, dual task (add armmovements or cognitive task)

Improve form and speed

terns of muscle recruitment limit func-tional mobility and eventually maj- re-sult in focal muscle weakness.

Because bradykinesia is due io im-paired central neural drive, rehabili-tation to reduce bradykinesia sbouldfocus on teaching patients to in-crease the speed, amplitude, andtemporal pacing of their self-initiatedand reactive limb and body center-of-mass (CoM) movements. Table 2presents representative exercisesaimed at reducing bradykinesia formobility. These exercises may pro-mote weight-shift control and pos-tural adjustments in anticipation ofvoluntary movements such as

lunges, kicks, and quick boxingmovements. Patients also practicetaking large, protective steps whiletilting past their limits of stability' andin response to external displace-ments associated with hitting orpunching a boxing bag. To reducebradykinesia. patients should be en-couraged to "think big" -* while in-creasing the speed and amplitude oflarge arm and leg mt)\'ement,sthroughout agility courses and dur-ing multidirectional lunges and box-ing (Tabs. 2 and 3). Walking sticksmay help patients attend to the lai^e,symmetrical arm swing that is coor-dinated with strides during gait.

FreezingFreezing of gait manifests as a move-ment hesitation in wliich a delay orcomplete inability to initiate a stepoccurs."'' Freezing not only slowswalking, but it also is a major con-tributor to falls in people with PI).""It is a poorly understood phenome-non that is associated with executivedisorders in people with PD."''""Freezing during gait occurs more of-ten when a person is negotiating acrowded environment or narrowdoorway, when making a turn, orwhen attention is diverted by a sec-ondan,' task."""''Jacobs and Horak""recently found tbat freezing or "starthesitation " 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

1

2

3

Surface

Sit on a chair

Sit on DynaDisc"

Stand on firm surface

Vision

Normal, well-lit room

Sunglasses

No-body glasses

Resistance

Holding pole

3-lb pole

6-ib pole

Dual Task

Counting

Verbal: make a list

Verbal/cognitive; math

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

Level

1

2

Speed/Agility

Self-paced

Increase speed

Quick changes in direction, pace,stop and go

Dual Task

Count steps out loud

Motor task; toss ball between hands

Cognitive task; math

Arms and Trunk (High Kneesand Tire Course Only)

Self-selected

Reciprocal arms

Add head and trunk rotation

C. Boxing: The hoxing task inciudes slmpie to complex combinations involving jabs, hooks, and crosses.

Level

1

2

3

Plane of Movement

Lateral stance to the bag

Pivot with back foot

Walk backward around bag

Speed

Self-paced

Bursts of speed; combo punches for 15 s

Bursts of speed: combo punches for 30 s

Dual Task

Count punches

Name punches (hook, jab, cross)

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.

Level

1

2

3

Surface

Firm surface

One foot on compliantsurface (DynaDisc/foam mat)

Foam mat (both feet)

External Cue

Rubber discsdesignate footplacement

Decrease disc sizeor number

No discs

Vision

Well-lit room

Sunglasses

No-body glasses

Resistance

No[ie

Weight vest (startwith 10% ofbody weight)

Increase vestweight, 5% ofbody weightincrements

Dual Task

None

Motor task; trunk

Verbal or cognitive

Arms and Trunk(Dynamic

Lunges Only)

None

Use armsreciprocally

Lift arms over headwhile holdingball

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

dated with repetitive, anticipatory,lateral weight shifts and that peoplewho are healthy can be made to"freeze" when they do not have timeto preplan which foot to use wheninitiating a compensator>' or volun-tary step. Therefore, freezing maybe related to difficulties in shifts ofattention, preplanning movementstrategies, or quickly selecting a cor-rect central motor program.

To help people in the early stages ofPD reduce their chances of heing

affected by freezing, agility exercisesshould be performed in environ-ments in which freezing typically oc-curs. As shown in Tables 2 and 3,exercises that involve high stepping,skipping, or taking large steps in dif-ferent directions through doorwaysand over and around obstacles, suchas between chairs placed shoulder-width apart, could potentially re-duce freezing episodes. Quick turnsshould he practiced in corners andnear walls. Individuals with PI) couldperform these exercises in the home

or gym, where obstacle courses havebeen set up that require turningquickly, negotiating narrow andtight spaces such as comers, duckingunder and stepping over obstacles,picking up objects while walking,and quickly changing directions andfoot placement. Once a person suc-cessfully performs the agility- exer-cises on an obstacle course, more-advanced progressions could beintroduced, such as performing dualcognitive task.s while maintainingform 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 andPoor Sequential CoordinationResearch suggests that the basal gan-glia play an imponant role in taskswitching, motor program selection,and suppression of irrelevant infor-mation before executing an action.' -The inability to quickly switch motorprograms has been demonstrated inindividuals with PD b) an inability tochange postural response synergiesin the first perturbation trial after achange in support, change in instruc-tions, or change in perturbation di-rection.^'"' Dopamine replacementdoes not improve inflexible programselection.'*2"^ The difficulty withswitching motor programs manifestsin difficulty maneuvering in new andchallenging environments and inchanges in postural transitions, suchas turning, standing irom a sittingposition, and rolling over.* * In addi-tion to difficulty switching motor¡irograms. people with FD have dif-ficulty sequencing motor ac-tions.''^ ""'«*' Patients with PD show adelay between their anticipator)'postural adjustments and voluntary-movements, such as rising ontotoes''** or a voluntary' step.*"'' Thesefindings suggest that mobility in peo-ple with PD is constrained by poorcoordination among body parts andbetween voluntary' movements andtheir associated postural adjust-ments, as well as by difficulty inswitching motor programs appropri-ate for changes in task constraints.

Consequently, an exercise programshould include complex, multiseg-mental. whole-body movements andshould include tasks requiring quickselection and sequencing of motorprograms such as practicing posturaltransitions (eg. moving from stanceto the floor, roiling, and arising fromthe floor to stance). As shown inTable 2, one such exercise approachis tai chi, wbich helps patients tolearn increasingly complex se-quences of movement and to focuson smooth timing and synchroniza-

tion of whole-body movements. In-corporating boxing actions into a re-membered sequence is another wayto practice tbe quick selection andsequencing of complex motor pro-grams for mobility. To address prol>lems of quick program selection,lunges and agility exercises also prt>vide practice changing motor strate-gies during stopping, starting, chang-ing direction, changing stepping limb,and changing the size and placementof steps.

Sensory IntegrationTbere is strong evidence that thebasal ganglia are critical for high-level integration of somatosensoryand visual information necessary toform an internal representation ofthe body and the environment.*^"""Despite clinical examinations of pa-tients with PD revealing only incon-sistent, subtle signs of abnormal sen-sory perception,""'"' an increasingnumber of studies are showing ab-normal kinesthesia and use of propri-oception in people with PD. For ex-ample. Wright et aP"* and Horak etal" found that individuals with PDhave an impaired ability to detect therotation of a surface or the passiverotation of the torso and tbat thispoor kinesthesia is worsened bylevodopa medication. Individualswith PD also show impaired percep-tion of arm position and movementand decreased response to musclevibration.' '-' ^ The poor use of pro-prioceptive information and de-creased perceptiiin of movement areassociated witb over-estimation ofbody motion (bradykinesia) andover-dependence on vision.'^"'"

To facilitate use of propdoceptiveinformation and reduce over-reliance on vision, an agility programshould progress balancing and walk-ing tasks by: (1) wearing dark sun-glasses to reduce visual contrast sen-sitivity and (2) use of "no body"glasses to obscure the bottom half ofthe visual field so the body cannot be

seen. In addition, many of the exer-cises can be performed on a varietyof surfaces to require adaptation toaltered somatosensory informationfrom the surface. External feedbackand sensory cues from the therapistregarding quality and size of themovements should be used initiallyand progressively decreased as pa-tients develop a more accurate inter-nal setise of body position. As shownin Table 3. the sensorimotor agilityprogram used as an example in thisarticle progresses with traditionalprogressive challenges"' (increasingresistance, speed of gait, endurance.atid so on) and witb sensorimotorchallenges (dual tasking and changesin base of support, visual input, andsurface conditions).

Cognitive ConstraintsThe inability to simultaneously carryout a cognitive task and a balance orwalking task has been found to be :ipredictor of falls in elderly people.'^'It is even more difficult for a personwitb PD tban age-matched elderlypeople to perform multiple tasks,"'~possibly because the basal gangliaare responsible for allowing auto-matic control of balance and gait andfor switching attention betweentasks.' -•"' ' Postural sway increasesmost in individuals with PD whohave a history of falls when a cogni-tive task is added to the task of quietstance."" These findings suggest thatthe ability to carry out a secondarycognitive or motor tasks while walk-ing or balancing is a critical elementof mobility that is a particular chal-lenge in people with PD.

An agility program could progresstask difficulty by adding cognitive ormottjr tasks tbat teach patients withPD to maintain postural stability dur-ing performance of secondary tasks.Table 5 presents exercises in wbichit is safe and appropriate to add adual cognitive or motor task. Ibeexercises at level 1 bave no dualtasks, 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 basieexercise such as an agility course,and level 3 has a cognitive task (eg,performing math or memor)' prob-lems) added to the same basic exer-cise. The progression of adding sec-ondary' tasks to gait and balance tasksserves as a training device as well asa tcM)I to help patients understand therelationship between safe mohilirj'and secondar>' tasks in everyday life.

A Sensorimotor AgilityProgram for PeopleWith PDIn this article, we propose a novelsensorimotor agility program tar-geted at constraints on mobility inpeople with PD. The expertise thatcontributed to the program includesan internationally recognized neurol-ogist specializing in movement disor-ders for more 3^ years and 5 physicaltherapists experienced in treatingpeople with PD, including 3 withPhDs with a focus on PD. Six certi-fied athletic trainers who regularlywork with people with PD also werehelpful in designing the program.We propose that the exercise pro-gram outlined in Table 2 could last60 minutes, with about 10 minvitesfor each category of exercise. Theexercises in the 6 categories wereselected to target one or more of theconstraints on mobility' (Tab. 1).

Although not all people witb PDhave all ot the constraints addressedin this article, it may be that exerciseshould target all of these constraints,as each constraint generally is asso-ciated with the progression of PDand eventually has a marked effecton mohilit)'. Addressing constraintsearly may delay the onset of relatedmobility deficits. Category' I, tai chi,"is a wliole-body exercise that focuseson developing a sense of body kines-thesia, improving postunil alignment,and sequencing of whole-bod> move-ments that move the CoM. CategoryII, "kayaking," focuses on trunk and

cervical rotation and speed, withlarge, coordinated arm movements.Category III, "agility- course," focuses()n quickly changing motor programssueh as quick turns, sequencing ac-tions, and overcoming freezing. Cat-egory IV, boxing,' focuses on build-ing the patient s agility and speed,backward walking, and componentsof anticipator)' and reactive posturaladjustments in response to a movinghag. Categor\' V. •'lunges," helps pa-tients with PD practice large CoMmovements, mtiltidirectit)nal limits ofstability, and steps for postural correc-tion. Category VI, pre-Pilates," is a setof exercises that help patients with PDextend and strengthen the spine, aswell as practice postural transitionssuch as sit-to-stand maneuvers, floortransfers, and rolling.'**

The sensorimotor progressions ofexercises II through V follow 3 levelsof difficulty (Tab. 3)- Progressions in-clude: (1) reducing the base ofsupport. (2) increasing surface com-pliance to reduce surface somato-sensor>' information for postural ori-entation, (3) increasing speed orresistance with weights. (4) addingsecondary cognitive tasks to auto-mate posture and gait, and (5) limit-ing visual input of the body with "nobody ' glasses or of the environmentwith dark sunglasses to increase useof kinesthetic information. Categor\'I (tai chi) and category VI (pre-Pilates) exercises progress by in-creasing the length of rememberedsequences and improving the formof each subcomponent of the move-ments. All of these sensorimotor pro-gressions were chosen spccificalh' totarget the predictable constraints onmobility- due to PD, and testing of theprogram is currently under way.

SummaryWe present a progressive sensorimo-tor agility exercise program for pre-vention of mobility disability in peo-ple with PD. The program is basedon the role of the basal ganglia in

posture and gait, the principles ofneural plasticity, and the inevitableconstraints of PD that ultimately af-fect dynamic balance and mobility.These principles of the program in-clude a focus on self-initiated move-ments, big and quick movements,large and flexible CoM control, re-ciprocal and coordinated move-ments of arms and legs, and rota-tional movements of ton>o overpelvis and pelvis over legs. Flexible,rotational axial motion of trunk andneck are stressed to achieve erectpostural alignment, strengthening ofextensors, and lengthening of Ilex-ors. Our program is designed to fa-cilitate sensory integration for bal-ance, emphasizing the use ofsomatosensory information to movethe body's CoM quickly and effec-tively for balance and mobility. Sec-ondary cognitive tasks are added tomobility tasks to automatize controlof balance and gait. This sensorimo-tor agility approach to mobility train-ing is intended for prevention of m obility disability^ but may be modifiedfor patients at later stages of PD p rogression to improve their mobility.

Both authors provided concept/idea/projectdesign, writing, and project management.Dr Horak provided fund procurement, facil-ities/equipment, institutional liaisons, andconsultation {including reviev f of manuscriptbefore submission),

The exercise program developed out ofbrainstorming sessions with the follovi/ingexpert neurologists, scientists, physical ther-apists, and trainers: Fay B Horak, PT, PhD, JayNutt, MD, Laurie A King, PT, PhD, Sue Scott,CT, Andrea Serdar, PT, CNS, Chad Swanson,CT, Valerie Kelly, PT, PhD, Ashley Scott, CT,David Vecto, CT, Triana Nagel-Nelson, CT,Kimberly Berg, CT, Nandini Deshpande, PT,PhD, and Cristiane Zampieri, PT, PhD. Straw-berry Gatts, PhD, provided expert advice toselect and modify tai chi moves for peoplewith Parkinson disease.

This work was supported by a grant from theKinetics Foundation and by a grant from theNational Institute on Aging (AG006457).

Dr Horak was a consultant for the KineticsFoundation. This potential conflict of interest

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 OregonHealth and Sciences University.

This article was received ¡uly 1 /, 2008, andwas accepted January 12, 2009.

DOI: 10.2522/ptj.20080214

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