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  • doi: 10.2522/ptj.20080214Originally published online February 19, 2009

    2009; 89:384-393.PHYS THER. Laurie A King and Fay B HorakProgramDisease Using a Sensorimotor Agility Exercise Delaying Mobility Disability in People With Parkinson

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

    This article introduces a new framework for therapists to develop an exerciseprogram to delay mobility disability in people with Parkinson disease (PD). Mobility,or the ability to efficiently navigate and function in a variety of environments, requiresbalance, agility, and flexibility, all of which are affected by PD. This article summa-rizes recent research identifying how constraints on mobility specific to PD, such asrigidity, bradykinesia, freezing, poor sensory integration, inflexible program selec-tion, and impaired cognitive processing, limit mobility in people with PD. 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 chi, kayaking, boxing, lunges, agilitytraining, and Pilates exercises, is presented. This new constraint-focused agilityexercise 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 mobilitypresented here can be incorporated into an ongoing or long-term exercise programfor people with PD.

    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 andBiomedical 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:[email protected].

    [King LA, Horak FB. Delaying mo-bility disability in people with Par-kinson disease using a sensorimo-tor agility exercise program. PhysTher. 2009;89:384393.]

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  • Most people who are diag-nosed with Parkinson dis-ease (PD) do not consultwith 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. Although there are excel-lent guidelines for physical thera-pists to treat patients with PD whoexhibit mobility problems in orderto improve or maintain their mobili-ty,1,2 there is little research onwhether exercise may delay or re-duce the eventual mobility disabilityin patients diagnosed with PD.

    The major cause of disability in peo-ple with PD is impaired mobility.3

    Mobility, the ability of a person tomove safely in a variety of environ-ments in order to accomplish func-tional tasks,4 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, which involves coordinationof complex sequences of move-ments, ongoing evaluation of envi-ronmental cues and contexts, theability to quickly switch motor pro-grams when environmental condi-tions change, and the ability to main-tain safe mobility during multiplemotor and cognitive tasks.5,6 Thetypes of mobility deficits inevitablewith the progression of PD suggest

    that the basal ganglia are critical forsensorimotor agility.2 Critical as-pects of mobility disability in peoplewith PD, such as postural instability,are unresponsive to pharmacologicaland surgical therapies,7 making pre-ventative exercise an attractive op-tion. As yet, there is no known on-going exercise program for peoplediagnosed with PD that focuses onmaintaining or improving their agil-ity to slow or reduce their decline inmobility.

    This 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 con-straints on mobility resulting frombasal ganglia degeneration. The sci-entifically 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 community. It is likelythat a mobility program, such 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 the 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,8 an increase in dopa-mine synthesis and release,9 and in-creased dopamine in the striatum fol-lowing acute bouts of exercise.10

    Such changes in the brain may affectbehavioral recovery as a result ofneuroplasticity (the ability of thebrain to make new synaptic connec-tions), neuroprotection, and slowingof neural degeneration.11,12 Studieswith parkinsonian rats have sug-gested that chronic exercise mayhelp reverse motor deficits in ani-mals by changing brain function.Specifically, rats that ran on a tread-mill showed preservation of dopami-nergic cell bodies and terminals11,13

    associated with improved runningdistance and speed,12 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.11

    Aerobic exercise, such as treadmilltraining and walking programs, hasbeen tested in individuals with PDand has been shown to improve gaitparameters, quality of life, and leva-dopa efficacy.1416 However, it is notclear whether aerobic training, byitself, is the best approach to improv-ing mobility, which depends upondynamic balance, dual tasking, nego-tiating complex environments, quickchanges 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 with

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  • PD if the therapist could incorporatetasks such as dual tasking, balancetraining, and set-switching into atreadmill program.

    There currently are many untestedexercise programs available for peo-ple with PD1719 as well as severalrandomized controlled studies thattest specific exercises, such asstrength (force-generating capacity)training or gait training.2029 The ap-proach presented in this article isfocused on exercises that challengesensorimotor control of dynamic bal-ance and gait to improve mobility inpeople with PD. There are manyother aspects of PD that also must beaddressed in rehabilitation.

    Drive NeuroplasticityWith Task-SpecificAgility ExerciseStudies in rats have demonstratedthat task-specific agility training (eg,acrobatic, environmental enrichment-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 such as run-ning on treadmills.3035 Task-specificexercise also has been shown to bemore effective than aerobic or gen-eral exercise to improve task perfor-mance in patients with stroke.36,37

    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-bility.18,22,3842 We have borrowedsingular techniques from several suc-cessful programs 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.43

    Nevertheless, the literature suggeststhat muscle weakness, secondary toabnormal muscle activation associ-ated with bradykinesia and rigidity,can be present at all stages ofPD.4447 Similarly, balance and mo-bility problems may be present inpeople with mild PD but only be-come apparent when more-complexcoordination is required under chal-lenging conditions.48,49 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.50,51 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 multi-segmental coordination.5254 Duringthe progression of PD, mobility isprogressively constrained by rigidity,bradykinesia, freezing, sensory inte-gration, inflexible motor programselection, and attention and cogni-tion.2 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 rigidity is characterizedby an increased resistance to passivemovement throughout the entirerange of motion, in both agonist andantagonist muscle groups.5557 Thefunctional outcomes of rigidity, ingeneral, include a flexed posture,58

    lack of trunk rotation,59,60 andreduced joint range of movementduring postural transitions andgait.56,61 Electromyography studieshave shown that people with PDhave high tonic background activity,especially in the flexors, and co-contraction of muscles during move-ment, especially in the axial mus-cles.56,57 In addition, antagonistmuscle activation is larger and ear-lier, resulting in coactivation of mus-cle groups during automatic posturalresponses.61

    Another characteristic of parkinso-nian rigidity is axial rigidity, whichresults in a loss of natural vertebral,pelvis/shoulder girdle, and femur/pelvis flexibility and range of motionthat accompanies efficient posturaland locomotor activities.60,62 Wrightet al55 found that rigidity 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 rigidity.55 The high axial tone(velocity-dependent resistance tostretch) in patients with PD contrib-utes to their characteristic en bloctrunk motions, which make it diffi-cult for them to perform activitiessuch as rolling over in bed or turningwhile walking.62

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  • Schenkman et al63 showed that ex-ercise can increase trunk flexibilityin people with PD. We proposean agility program that includesmovements that minimize agonist-antagonist muscle co-contraction (ie,reciprocal movements), promote ax-ial rotation, lengthen the flexor mus-cles, and strengthen the extensormuscles to promote an erect pos-ture. Rigidity can potentially be ad-dressed with kayaking, an exercisein which the person counter-rotatesthe shoulder and pelvic girdle; taichi, a set of exercises that focuses onthe individuals awareness of pos-tural alignment during postural tran-sitions; and pre-Pilates, a series ofexercises aimed at increasing spinalmobility and lengthening flexor mus-cles groups. In addition, the programshould include strategies for turningand transitioning from a standing po-sition to sitting on the floor and backagain that emphasize trunk and headrotation (Tabs. 2 and 3).18

    BradykinesiaBradykinesia is most commonly de-fined as slowness of voluntary move-ment,43 but it also is associated withslow and weak postural responses toperturbations and anticipatory pos-tural adjustments. Reactive posturalresponses to surface translations61,64

    and anticipatory postural movementsprior to rising onto toes65 and priorto step initiation66 are bradykineticin patients with PD. Bradykinetic vol-untary stepping and postural com-pensatory stepping are characterizedby a delayed time to lift the swinglimb, a weak push-off, reduced leg lift,a small stride length, and lack of armswing.61,64,66,67 Bradykinesia also isapparent in reduced voluntary andreactive limits of stability, especiallyin the backward direction.64,68 Thecharacteristic narrow stance of pa-tients with PD may be compensatoryfor bradykinetic anticipatory posturaladjustments prior to a step, at theexpense of reduced lateral posturalstability.67,69 Bradykinetic postural

    responses in people with PD gener-ally are not improved by antiparkin-sonian medications, highlighting theneed for an exercise approach to thisconstraint on mobility.6 Bradykinesiaalso is seen in postural transitions suchas turning70 and the supine-to-standmanuever,59 as well as in single-jointmovements71 and multi-joint reachingmovements72 in people with PD.

    Bradykinesia is evident in slowedrate of increase and decrease of mus-cle activation patterns.73 Reductionin muscle strength in people with PDhas been attributed primarily to re-duced cortical drive to muscles be-cause voluntary contraction, but notmuscle response to nerve stimula-tion, is weak in these individuals.74,75

    Electromyographic activity in bradyki-netic muscles often is fractionated intomultiple bursts and is not well scaledfor changes in movement distance orvelocity.71 Years of bradykinesia fromabnormal, centrally driven musclecontrol and abnormal, inefficient pat-

    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-contractionFlexed alignment of trunkReduced trunk rotationReduced joint range of movementHigh axial tone (stiffness)

    Trunk rotationReciprocal movementsRhythmic movementsErect alignmentLarge CoM movementsIncrease limits of stability

    II. Bradykinesia Slow, small movementsNarrow base of supportLack of arm swing

    Fast, large stepsCoM controlLarge arm swings

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

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

    IV. Inflexible program selection(sequential coordination)

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

    Plan task in advanceQuick change strategiesSequencing components of task

    V. Impaired sensory integration Inaccurate without visionImbalance on unstable surfacePoor alignment with environment

    Kinesthetic awarenessDecrease surface dependenceFlexible orientation

    VI. Reduced executive functionand attention

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

    a CoMcenter of mass.

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

    Because bradykinesia is due to im-paired central neural drive, rehabili-tation to reduce bradykinesia shouldfocus 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 big42 while in-creasing the speed and amplitude oflarge arm and leg movementsthroughout agility courses and dur-ing multidirectional lunges and box-ing (Tabs. 2 and 3). Walking sticksmay help patients attend to the large,symmetrical arm swing that is coor-dinated with strides during gait.

    FreezingFreezing of gait manifests as a move-ment hesitation in which a delay orcomplete inability to initiate a stepoccurs.76 Freezing not only slowswalking, but it also is a major con-tributor to falls in people with PD.77

    It is a poorly understood phenome-non that is associated with executivedisorders in people with PD.76,78

    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-ondary task.77,79 Jacobs and Horak80

    recently found that freezing or starthesitation in step initiation is asso-

    Table 2.Representative Agility Exercise Program, With Progressions

    Exercise Actions Progressions

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

    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 horses mane: coordination of arms

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

    walking, with diagonal weight shifts

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

    II. Kayaking: Trunk rotation,segmental coordination, speed

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

    Speed, surface, resistance, vision, dual task

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

    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

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

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

    Jab: 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

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

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

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

    Single multidirectional steps (clock stepping)Dynamic multidirectional lunge walking

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

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

    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

    Improve form and speed

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  • ciated with repetitive, anticipatory,lateral weight shifts and that peoplewho are healthy can be made tofreeze when they do not have timeto preplan which foot to use wheninitiating a compensatory 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 being

    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 be practiced in corners andnear walls. Individuals with PD couldperform these exercises in the home

    or gym, where obstacle courses havebeen set up that require turningquickly, negotiating narrow andtight spaces such as corners, 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 tasks while maintainingform and speed on agility tasks.

    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 kneeswalking with hands touching knees, skipping, lateral shuffles, grapevine, and tire course. Advanced individuals may addagility on an inclined surface and bouncing or tossing a ball.

    Level Speed/Agility Dual TaskArms and Trunk (High Knees

    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,stop and go

    Cognitive task: math Add head and trunk rotation

    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.

    Level Surface External Cue Vision Resistance Dual Task

    Arms and Trunk(Dynamic

    Lunges Only)

    1 Firm surface Rubber discsdesignate footplacement

    Well-lit room None None None

    2 One foot on compliantsurface (DynaDisc/foam mat)

    Decrease disc sizeor number

    Sunglasses Weight vest (startwith 10% ofbody weight)

    Motor task: trunk Use armsreciprocally

    3 Foam mat (both feet) No discs No-body glasses Increase vestweight, 5% ofbody weightincrements

    Verbal or cognitive Lift arms over headwhile holdingball

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

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  • Inflexible Program Selection andPoor Sequential CoordinationResearch suggests that the basal gan-glia play an important role in taskswitching, motor program selection,and suppression of irrelevant infor-mation before executing an action.52

    The inability to quickly switch motorprograms has been demonstrated inindividuals with PD by an inability tochange postural response synergiesin the first perturbation trial after achange in support, change in instruc-tions, or change in perturbation di-rection.51,81 Dopamine replacementdoes not improve inflexible programselection.82,83 The difficulty withswitching motor programs manifestsin difficulty maneuvering in new andchallenging environments and inchanges in postural transitions, suchas turning, standing from a sittingposition, and rolling over.84 In addi-tion to difficulty switching motorprograms, people with PD have dif-ficulty sequencing motor ac-tions.65,85,86 Patients with PD show adelay between their anticipatorypostural adjustments and voluntarymovements, such as rising ontotoes65 or a voluntary step.66 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, rolling, and arising fromthe floor to stance). As shown inTable 2, one such exercise approachis tai chi, which 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 the quick selection andsequencing of complex motor pro-grams for mobility. To address prob-lems of quick program selection,lunges and agility exercises also pro-vide practice changing motor strate-gies during stopping, starting, chang-ing direction, changing stepping limb,and changing the size and placementof steps.

    Sensory IntegrationThere 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.87,88

    Despite clinical examinations of pa-tients with PD revealing only incon-sistent, subtle signs of abnormal sen-sory perception,89,90 an increasingnumber of studies are showing ab-normal kinesthesia and use of propri-oception in people with PD. For ex-ample, Wright et al55 and Horak etal64 found that individuals with PDhave an impaired ability to detect therotation of a surface or the passiverotation of the torso and that thispoor kinesthesia is worsened bylevodopa medication. Individualswith PD also show impaired percep-tion of arm position and movementand decreased response to musclevibration.9193 The poor use of pro-prioceptive information and de-creased perception of movement areassociated with over-estimation ofbody motion (bradykinesia) andover-dependence on vision.50,94

    To facilitate use of proprioceptiveinformation 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 bodyglasses 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 sense of body position. As shownin Table 3, the sensorimotor agilityprogram used as an example in thisarticle progresses with traditionalprogressive challenges95 (increasingresistance, speed of gait, endurance,and so on) and with 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 apredictor of falls in elderly people.96

    It is even more difficult for a personwith PD than age-matched elderlypeople to perform multiple tasks,86

    possibly because the basal gangliaare responsible for allowing auto-matic control of balance and gait andfor switching attention betweentasks.52,86 Postural sway increasesmost in individuals with PD whohave a history of falls when a cogni-tive task is added to the task of quietstance.97 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 ormotor tasks that teach patients withPD to maintain postural stability dur-ing performance of secondary tasks.Table 3 presents exercises in whichit is safe and appropriate to add adual cognitive or motor task. Theexercises at level 1 have no dualtasks, level 2 has a motor task (eg,

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  • bouncing a ball) added to the basicexercise such as an agility course,and level 3 has a cognitive task (eg,performing math or memory 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 tool to help patients understand therelationship between safe mobilityand secondary 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 35 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 minutesfor 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 with PDhave all of 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 mobility. Addressing constraintsearly may delay the onset of relatedmobility deficits. Category I, tai chi,is a whole-body exercise that focuseson developing a sense of body kines-thesia, improving postural alignment,and sequencing of whole-body move-ments that move the CoM. CategoryII, kayaking, focuses on trunk and

    cervical rotation and speed, withlarge, coordinated arm movements.Category III, agility course, focuseson quickly changing motor programssuch as quick turns, sequencing ac-tions, and overcoming freezing. Cat-egory IV, boxing, focuses on build-ing the patients agility and speed,backward walking, and componentsof anticipatory and reactive posturaladjustments in response to a movingbag. Category V, lunges, helps pa-tients with PD practice large CoMmovements, multidirectional 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.18

    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-sensory 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. CategoryI (tai chi) and category Vl (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 specifically 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 torso overpelvis and pelvis over legs. Flexible,rotational axial motion of trunk andneck are stressed to achieve erectpostural alignment, strengthening ofextensors, and lengthening of flex-ors. Our program is designed to fa-cilitate sensory integration for bal-ance, emphasizing the use ofsomatosensory information to movethe bodys 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 mo-bility disability but may be modifiedfor patients at later stages of PD pro-gression 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 review of manuscriptbefore submission).

    The exercise program developed out ofbrainstorming sessions with the followingexpert 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

    A Sensorimotor Agility Exercise Program for People With Parkinson Disease

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  • has been reviewed and managed by OregonHealth and Sciences University.

    This article was received July 11, 2008, andwas accepted January 12, 2009.

    DOI: 10.2522/ptj.20080214

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  • doi: 10.2522/ptj.20080214Originally published online February 19, 2009

    2009; 89:384-393.PHYS THER. Laurie A King and Fay B HorakProgramDisease Using a Sensorimotor Agility Exercise Delaying Mobility Disability in People With Parkinson

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