Experimental Results Using Force-Feedback Cueing in Robot-Assisted Stroke Therapy

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IEEE TRANSACTIONS ON NEURAL SYSTEMS AND REHABILITATION ENGINEERING, VOL. 13, NO. 3, SEPTEMBER 2005 335 Experimental Results Using Force-Feedback Cueing in Robot-Assisted Stroke Therapy Michelle J. Johnson, Member, IEEE, H. F. Machiel Van der Loos, Member, IEEE, Charles G. Burgar, Member, IEEE, Peggy Shor, and Larry J. Leifer, Member, IEEE Abstract—Stroke is the leading cause of disability among adults in the United States. Behaviors such as learned nonuse hinder hemiplegic stroke survivors from the full use of both arms in activ- ities of daily living. Active force-feedback cues, designed to restrain the use of the less-affected arm, were embedded into a meaningful driving simulation environment to create robot-assisted therapy device, driver’s simulation environment for arm therapy (SEAT). The study hypothesized that force-feedback control mode could “motivate” stroke survivors to increase the productive use of their impaired arm throughout a bilateral steering task, by providing motivating feedback and reinforcement cues to reduce the overuse of the less-affected arm. Experimental results demonstrate that the force cues counteracted the tendency of hemiplegic subjects to produce counter-productive torques only during bilateral steering tasks ( ) that required the movement of their impaired arm in steering directions up and against gravity. Impaired arm activity was quantified in terms of torques due to the measured tangential forces on the split-steering wheel of driver’s SEAT during bilateral steering. Results were verified using surface electromyograms recorded from key muscles in the impaired arm. Index Terms—Constraint-induced movement therapy, hemi- plegia, rehabilitation, robotics, stroke. I. INTRODUCTION I N CHARACTERIZING the goal of stroke rehabilitation therapy for hemiplegia, Eggers [1] states, “the conscious use of the paralyzed hand should not be the end goal of … therapy. The goal should be the spontaneous use of both hands. Only this ability is useful for the patient in everyday life” ([1, p. 34]). In this spirit, this investigation aimed to evaluate, within the context of a simple steering task that mimics real driving, a novel force-feedback and reinforcement strategy aimed at Manuscript received December 19, 2002; revised February 24, 2005. This work was supported in part by the Veterans Health Care System Rehabilita- tion Research and Development Center under Grant B2257PA and in part by the National Aeronautics and Space Administration-AMES Center under Grant 2-52208. M. J. Johnson is with the Department of Physical Medicine and Rehabili- tation, Medical College of Wisconsin, Milwaukee, WI 53226 USA, and also with the Marquette Rehabilitation Robotics Research and Design Laboratory, Department of Biomedical Engineering, Marquette University, Milwaukee, WI 53226 USA (e-mail: [email protected]). H. F. M. Van der Loos and P. Shor are with the Rehabilitation Research and Development Center, Veterans Affairs Medical Center, Palo Alto, CA 94304- 1200 USA (e-mail: [email protected]; [email protected]). C. G. Burgar is with Physical Medicine and Rehabilitation, Central Texas Veterans Affairs Health Care System, Temple, TX 76504 USA (e-mail: [email protected]). L. J. Leifer is with the Department of Mechanical Engineering, Design Divi- sion, Stanford Center for Design Research Center for Design Research, Stanford University, Stanford, CA 94305-2232 USA (e-mail: [email protected]). Digital Object Identifier 10.1109/TNSRE.2005.850428 limiting the tendency of stroke survivors with hemiparesis to overuse their less-affected arm. Stroke is the leading cause of disability among adults in the United States [2]. Most reports on risk factors for stroke list “old age” as the strongest determinant of incidence [3]. This is alarming when viewed in terms of current U.S. demographic trends, which show that individuals over 65 years are the fastest growing segment of our population [4]. Many stroke survivors with upper arm hemiparesis exhibit maladaptive behaviors that are typically characterized by overuse of the less-affected arm and underuse of the impaired arm in activities of daily living (ADL) [5]–[13]. These behaviors may be the result of psychological factors, as well as physical and cognitive ones such as impairment of motor function and motor planning ca- pacities. One common maladaptive behavior, learned nonuse, is characterized as a psychological barrier that hinders stroke sur- vivors from using their impaired arm even in the face of latent functional ability. Given these realities, we believe that there is a need for robotic therapy devices that implement creative feedback strategies to assist stroke survivors with hemiplegia to overcome the tendency to overuse their less-affected arm in real environments. The rising cost of healthcare has forced many rehabilitation environments to be characterized by low therapist-to-patient ratios with heavy reliance on outpatient rehabilitation [2]. When these treatment conditions are juxtaposed against recent research suggesting that recovery from stroke is maximized in environments where patients can receive one-on-one, intense, repetitive therapy the need for affordable therapy assistants emerges. The development of robotic devices that can function as low-cost assistants to therapists and permit patients to do autonomous and semi-autonomous training emerges as one possible solution. It is hypothesized that force-feedback embedded into a low- cost, meaningful simulation environment can be used to create a robot-assisted therapy device that can assist stroke survivors with hemiplegia to decrease the overuse of the less-affected arm and increase the use of their impaired arm in a functional bi- lateral steering task. A forced-use feedback and reinforcement scheme was implemented to provide stronger reasons to use the impaired arm. This paper reports on experimental results that demonstrate that as a result of the presence of the force cues, subjects were able to significantly increase the productive use of their impaired arm in the bilateral steering tasks. Impaired arm use is quantified in terms of torques due to measured tan- gential forces on the split-steering wheel of driver’s simulation environment for arm therapy (SEAT) during bilateral steering. Results were verified using surface electromyograms (sEMG) recorded from key muscles in the impaired arm. 1534-4320/$20.00 © 2005 IEEE

Transcript of Experimental Results Using Force-Feedback Cueing in Robot-Assisted Stroke Therapy

IEEE TRANSACTIONS ON NEURAL SYSTEMS AND REHABILITATION ENGINEERING, VOL. 13, NO. 3, SEPTEMBER 2005 335

Experimental Results Using Force-FeedbackCueing in Robot-Assisted Stroke Therapy

Michelle J. Johnson, Member, IEEE, H. F. Machiel Van der Loos, Member, IEEE, Charles G. Burgar, Member, IEEE,Peggy Shor, and Larry J. Leifer, Member, IEEE

Abstract—Stroke is the leading cause of disability among adultsin the United States. Behaviors such as learned nonuse hinderhemiplegic stroke survivors from the full use of both arms in activ-ities of daily living. Active force-feedback cues, designed to restrainthe use of the less-affected arm, were embedded into a meaningfuldriving simulation environment to create robot-assisted therapydevice, driver’s simulation environment for arm therapy (SEAT).The study hypothesized that force-feedback control mode could“motivate” stroke survivors to increase the productive use of theirimpaired arm throughout a bilateral steering task, by providingmotivating feedback and reinforcement cues to reduce the overuseof the less-affected arm. Experimental results demonstrate thatthe force cues counteracted the tendency of hemiplegic subjects toproduce counter-productive torques only during bilateral steeringtasks (p 0 05) that required the movement of their impairedarm in steering directions up and against gravity. Impaired armactivity was quantified in terms of torques due to the measuredtangential forces on the split-steering wheel of driver’s SEATduring bilateral steering. Results were verified using surfaceelectromyograms recorded from key muscles in the impaired arm.

Index Terms—Constraint-induced movement therapy, hemi-plegia, rehabilitation, robotics, stroke.

I. INTRODUCTION

I N CHARACTERIZING the goal of stroke rehabilitationtherapy for hemiplegia, Eggers [1] states, “the conscious

use of the paralyzed hand should not be the end goal of …therapy. The goal should be the spontaneous use of both hands.Only this ability is useful for the patient in everyday life” ([1, p.34]). In this spirit, this investigation aimed to evaluate, withinthe context of a simple steering task that mimics real driving,a novel force-feedback and reinforcement strategy aimed at

Manuscript received December 19, 2002; revised February 24, 2005. Thiswork was supported in part by the Veterans Health Care System Rehabilita-tion Research and Development Center under Grant B2257PA and in part bythe National Aeronautics and Space Administration-AMES Center under Grant2-52208.

M. J. Johnson is with the Department of Physical Medicine and Rehabili-tation, Medical College of Wisconsin, Milwaukee, WI 53226 USA, and alsowith the Marquette Rehabilitation Robotics Research and Design Laboratory,Department of Biomedical Engineering, Marquette University, Milwaukee, WI53226 USA (e-mail: [email protected]).

H. F. M. Van der Loos and P. Shor are with the Rehabilitation Research andDevelopment Center, Veterans Affairs Medical Center, Palo Alto, CA 94304-1200 USA (e-mail: [email protected]; [email protected]).

C. G. Burgar is with Physical Medicine and Rehabilitation, Central TexasVeterans Affairs Health Care System, Temple, TX 76504 USA (e-mail:[email protected]).

L. J. Leifer is with the Department of Mechanical Engineering, Design Divi-sion, Stanford Center for Design Research Center for Design Research, StanfordUniversity, Stanford, CA 94305-2232 USA (e-mail: [email protected]).

Digital Object Identifier 10.1109/TNSRE.2005.850428

limiting the tendency of stroke survivors with hemiparesis tooveruse their less-affected arm.

Stroke is the leading cause of disability among adults in theUnited States [2]. Most reports on risk factors for stroke list“old age” as the strongest determinant of incidence [3]. This isalarming when viewed in terms of current U.S. demographictrends, which show that individuals over 65 years are the fastestgrowing segment of our population [4]. Many stroke survivorswith upper arm hemiparesis exhibit maladaptive behaviorsthat are typically characterized by overuse of the less-affectedarm and underuse of the impaired arm in activities of dailyliving (ADL) [5]–[13]. These behaviors may be the result ofpsychological factors, as well as physical and cognitive onessuch as impairment of motor function and motor planning ca-pacities. One common maladaptive behavior, learned nonuse, ischaracterized as a psychological barrier that hinders stroke sur-vivors from using their impaired arm even in the face of latentfunctional ability. Given these realities, we believe that thereis a need for robotic therapy devices that implement creativefeedback strategies to assist stroke survivors with hemiplegiato overcome the tendency to overuse their less-affected arm inreal environments.

The rising cost of healthcare has forced many rehabilitationenvironments to be characterized by low therapist-to-patientratios with heavy reliance on outpatient rehabilitation [2].When these treatment conditions are juxtaposed against recentresearch suggesting that recovery from stroke is maximized inenvironments where patients can receive one-on-one, intense,repetitive therapy the need for affordable therapy assistantsemerges. The development of robotic devices that can functionas low-cost assistants to therapists and permit patients to doautonomous and semi-autonomous training emerges as onepossible solution.

It is hypothesized that force-feedback embedded into a low-cost, meaningful simulation environment can be used to createa robot-assisted therapy device that can assist stroke survivorswith hemiplegia to decrease the overuse of the less-affected armand increase the use of their impaired arm in a functional bi-lateral steering task. A forced-use feedback and reinforcementscheme was implemented to provide stronger reasons to use theimpaired arm. This paper reports on experimental results thatdemonstrate that as a result of the presence of the force cues,subjects were able to significantly increase the productive useof their impaired arm in the bilateral steering tasks. Impairedarm use is quantified in terms of torques due to measured tan-gential forces on the split-steering wheel of driver’s simulationenvironment for arm therapy (SEAT) during bilateral steering.Results were verified using surface electromyograms (sEMG)recorded from key muscles in the impaired arm.

1534-4320/$20.00 © 2005 IEEE

336 IEEE TRANSACTIONS ON NEURAL SYSTEMS AND REHABILITATION ENGINEERING, VOL. 13, NO. 3, SEPTEMBER 2005

II. BACKGROUND

Robot-assisted environments [14]–[19] are useful toolsin stroke rehabilitation. Typically, they facilitate objectiveassessment of impairment and implement protocols that ad-dress mainly biomechanical barriers to functional restoration,such as muscle incoordination and motor impairment. Fewrobot-assisted therapy environments have implemented mech-anisms that systematically address the psychological barriersto bilateral function. Most environments do not optimize forbilateral functioning or provide training to help patients copewith behaviors that hinder it.

Constraint-induced (CI) movement therapy (nonde-vice-based therapy) provides a viable method for improving theability of robot-assisted therapy to address the psychologicalfactors that hinder bilateral function on ADLs. CI presentsa therapy solution that creates additional reasons for chronichemiplegic patients to use their impaired upper arm in func-tional activities [5]–[9]. Typically in CI therapy techniques,therapists use passive devices (e.g., a sling or glove) to re-strain the less-affected arm. Evidence suggests that passiverestraint of the less-affected arm coupled with therapy requiringuse of the impaired arm in ADLs provide patients with thefeedback needed to overcome learned nonuse behavior. Thesling adds the reinforcement needed to help discourage use ofthe less-affected arm by acting to reduce patients’ behavioraloptions. This reduction is especially important in unsupervisedenvironments.

Studies indicate that CI therapy improves motor function inthe upper arm and, at the same time, produces use-dependentcortical reorganization leading to some permanent gains in func-tional use of the impaired arm in bilateral and unilateral real-world activities [5]–[12]. In a review of clinical trials usingCI therapy, Taub et al. [6] suggests that the main therapeuticfactor of the CI therapy interventions is the repetitive use ofthe impaired arm. More recent studies suggest that repeated,task-specific practice plays a role in reacquisition of motor func-tion while the intensity of scheduled practice is less important[6], [10]–[12]. Functional magnetic resonance imaging (FMRI)studies are beginning to suggest that the use-dependent corticalreorganization that takes place in the CNS after the therapy maybe rooted into the engaging, task-specific and skill developingfocus of the training [12]. Additional large scale, randomizedstudies are needed to assess the effectiveness of CI therapy (ad-ministered for 6 hours a day for two weeks) and modified ver-sions of CI therapy (administered three times a week for 6–10weeks) in reducing motor impairment and increasing carryoverto the real-world. Although the restraint may play an importantrole, its effect as a factor still needs to be determined.

Constraint-Induced treatment is criticized for having a pro-tocol that is unrealistic in today’s rehabilitation clinics wheretherapists have many patients and physical and occupationtherapy sessions last for only 30–60 min per day. Although theone-on-one, 6 h per day protocol is demanding and exceedscurrent practice, the evidence supports the possible effective-ness of CI therapies. Therefore, it is important to find practicalways to implement it [8], [13]. One practical way is to modifythe schedule demand, while another is to enable more semi-au-tonomous training.

Fig. 1. Driver’s SEAT system is shown on the left. Subject is positioned at thewheel with both arms in the bilateral steering position. Tracking task is on thedisplay monitor and appears similar to the graphic shown in the small figure inthe middle. Subject’s arm is instrumented with surface electrodes. Figure on theright shows a close up look at the Nicolet II amplifier with surface electrodes onthe biceps brachii and middle deltoid. Video markers (small balls) can be seenon the subject’s shoulder.

The force-cue mode embedded into a driving simulationenvironment, such as driver’s SEAT enables us to examinepossibilities for task-specific, semi-autonomous training thatprovides opportunities for patient-initiated, repeated prac-tice. Automating aspects of the restraint concepts of CI therapywithin driver’s SEAT leads us to a type of robot-assisted therapythat brings some forced-use aspects of CI therapy to rehabili-tation environments characterized by low therapist-to-subjectratios and limited interaction between subject and therapistduring training sessions. An automated restraint could poten-tially provide a foolproof method to discourage overuse of theless-affected arm in under-supervised or unsupervised bilateraltraining activities. Fig. 1 shows a subject using driver’s SEAT[19], [20].

In the driver’s SEAT environment, we use force reflectionto partially restrain the strong arm. Partial restraint is accom-plished using corrective force cues defined as the stiffening ofthe wheel in proportion to the stronger arm’s tangential force onthe wheel rim. One important difference between the force cuereminders used by driver’s SEAT and the restraining strategyof CI therapy strategy is in the management of reinforcement.While performing a task, if a stroke patient tries to use theless-affected hand, a bulky glove reminds (cue) them to not doso [6], [7]. If the patient ignores the reminder, the physical thera-pist intervenes with a verbal encouragement to use the impairedlimb. In contrast, in our implementation, the reminder is thestiffening of the wheel in proportion to the strong arm’s use;a cue which by disrupting the subject’s ability to easily controlthe wheel should lead to immediate awareness of strong arm’suse and corrective action.

The research question addressed in this pilot study is whetherthe corrective force cues caused a significant increase in the“use” of the impaired arm. The increased use of the impairedarm is determined by assessing its directionally appropriate con-tribution to the steering task. The performances of the impairedarm of hemiplegic and the nondominant arm of neurologicallyintact subjects (control subjects) during bilateral steering tasksunder conditions with force cues and without force cues areevaluated. In the ensuing discussion, weak arm (WA) will referto both the weaker impaired arm of hemiplegic subjects and thenondominant arm of control subjects. Strong arm (SA) will refer

JOHNSON et al.: EXPERIMENTAL RESULTS USING FORCE-FEEDBACK CUEING IN ROBOT-ASSISTED STROKE THERAPY 337

to the stronger less-affected arm of stroke subjects and the dom-inant arm of control subjects.

The impact of the force cues on the weak arm is primarilyevaluated using a metric that is based on the amount of torquethe arm produces (about the wheel’s hub) during steering.The upper body postural activity of hemiplegic subjects wasanalyzed along with the muscle activity (sEMG) recorded frommuscles in the weak arm of all subjects to help qualify anychanges observed in the impaired arm’s torque productionduring steering. The weak arm of hemiplegic subjects is com-pared to the weak arm of control subjects to determine whichwas more significantly impacted by the force cues.

III. FORCE CUE EXPERIMENT

It was hypothesized that the presence of force cues during bi-lateral steering would reduce the overuse of the SA, and causesubjects to rely more on their WA to appropriately complete thetracking task. Increased use of the WA was expected to corre-spond to productive WA torque activity, i.e., torques in the samedirection as the steering movement. Since control subjects werenot expected to use their SA in a maladaptive manner, we ex-pected that the effect of the force cues on the participation of theWA would be greater for hemiplegic subjects than for controls.It was also hypothesized that since EMG activity was related toforce production [21], the presence of force cues would causesignificant increases in the WA muscle activity levels for upperarm muscles that are primarily responsible for the steering task[22]–[24].

We anticipated that the presence of the force cues may causehemiplegic subjects with low motor function to attempt to usepostural adjustments to aid their WA to complete rotations of thesteering wheel. Cirstea and Levin [25], as well as Ada et al. [26]showed that neurologically impaired subjects with severe motorimpairment often recruited their trunk to help them completea reaching task requiring movements across the body (towardthe less-affected side and away from their impaired side). Weexamined postural activity to determine if increases in WA taskinvolvement were due to increases in muscle activity due to theforced-use of WA and not just postural adjustments.

A. Apparatus and Conditions

Driver’s SEAT (Fig. 1) was used as the experimental ap-paratus for this study; it is discussed in detail in [19] and[20]. Driver’s SEAT consists of a car-steering simulation thatis presented via a graphical interface that is interfaced to asplit-steering wheel, which is able to measure the left and righttangential forces on the wheel rim. Subjects were seated approx-imately 1.0 m away from the monitor. The wheel was tiltedradians from vertical. The steering wheel height was adjustedto ensure a comfortable interaction with the steering wheelthroughout the range of motion. During this experiment, themaximum torque that could be commanded to oppose measuredtangential forces on the wheel rim was limited to 4.5 Nm, i.e.,the maximum tangential force that could be resisted was 24.5 N.

The torque experienced at the wheel was generated using theformulas shown in Table I. The desired torque changed witheach mode and was used to create the different feedback effects

TABLE IDESIRED TORQUES ON WHEEL IN STEERING MODES

Where the desired control laws were functions of: qthe wheel angular position; _q the wheel angular ve-locity; and, in the case of the force-cue condition Tthe torque from the SA limb.

at the wheel. A proportional-derivative control law was usedin the no force-cue mode to provide a spring-damper restoringtorque that drove the wheel position ( ) back to zero when itwas perturbed. The extra term added to the control law in theforce-cue condition approximated the torque from the SA limb( ); this term, provided, in the closed loop condition, the pro-portional stiffening of the wheel. In our control, the force-cueterm was implemented as a feed-forward term.

Subjects followed a designated line on a moving road scene(see Fig. 1). Steering the desired road required rotating thesteering wheel approximately radians. The same threedistinct curvatures existed within all variations of the roadscenery; these defined three 15-s-long subtasks: a right turn(RT), a straight track (ST), and a left turn (LT), plus an initial5-s transitioning strip. Subjects were required to steer theroads under force-cue and no force-cue conditions using oneof two types of limb interactions: bilateral (two hands on thewheel) or unilateral (one hand (WA or SA) on the wheel); thiscombination defined a steering task.

B. Methods

1) Subjects: Tables II and III summarize the data for the six-teen subjects who participated in this study. Eight subjects hadhemiplegia: four subjects had right-hemiplegia (RH) and fourhad left hemiplegia (LH). Their ages ranged from 51 to 81 yearsold with a mean age of years. All hemiplegicsubjects had a right-sided, prestroke dominance. A total of eightneurologically intact subjects (mean age: years)participated in the study. The four right-hand dominant subjects(LNs) were controls for the left hemiplegic subjects while thefour left-hand dominant subjects (RNs) were controls for theright hemiplegic subjects. Hemiplegic subjects were includedif they met the following conditions: they were more than1 year post-stroke or after the appearance of hemiplegia instable cardiovascular, orthopedic, and neurological condition,as assessed by a physician and self-reported via a prescreenquestionnaire; they had minimal cognitive impairment with anoverall average score on the Neurobehavioral Cognitive StatusExam (NCSE or COGNISTAT) [2], [27]; they had a wide rangeof muscle tone and voluntary control with minimum upperextremity motor score of 20 on the upper extremity motorcontrol portion of the Fugl–Meyer (UE F-M) assessment test[2], [28], [29]; and had experience in real world driving prior todisability (self-reported).

2) Procedure: First, an occupational therapist preparedeach subject’s WA with surface electrodes to monitor muscleactivity during steering. Surface electrodes were used to recordthe sEMG activity of seven upper limb muscles (see Table IV).

338 IEEE TRANSACTIONS ON NEURAL SYSTEMS AND REHABILITATION ENGINEERING, VOL. 13, NO. 3, SEPTEMBER 2005

TABLE IIHEMIPLEGIC SUBJECTS PROFILE DATA

TABLE IIICONTROL SUBJECTS PROFILE DATA

These seven muscles were chosen because they are wholly orpartially responsible for key movements observed to be criticalto the steering tasks [22]–[24]. A pair of surface electrodeswere placed 2 cm apart over the chosen muscles of WA (Fig. 1).Preparation of the skin and the location of these electrodeswere done according to the procedures outlined in surfaceEMG placement guides [30]. A ground reference electrode wasplaced on the olecranion process (elbow). The electrodes weretaped securely to the skin and kept in place throughout thesession.

In this study, subjects drove with their hands in a fixed posi-tion on the wheel. Afterwards, subjects were seated in a wheel-chair and informed of the emergency stop and the safety featureson driver’s SEAT. They were asked to place their hands at desig-nated positions (approximately radians from top center)on the steering wheel. Both arms were placed in the followingposition: forearms neutral, elbows flexed to about radians,and shoulders slightly abducted and flexed. They were informedthat this position was the standard bilateral steering position.

Markers were placed on the wheel to indicate the correct handpositions. In addition, the therapist and the experimenter pro-vided the reminders, which enabled subjects to duplicate the

TABLE IVLIST OF THE MUSCLES MONITORED VIA SURFACE ELECTRODES

During contralateral rotations of the wheel, the arm is thoughtto mainly undergo flexion, internal rotation, and abduction atthe shoulder, extension of the elbow, as well as elevation of theshoulder. On the other hand, during ipsilateral rotations of thewheel, the arm is thought to mainly undergo extension at theshoulder, adduction of the arm in front of the trunk while stillinternally rotated, flexion of the elbow, as well as depression of theshoulder.

standard position each time they were required to replace andremove their hands on the wheel. If a subject had difficultygrasping the wheel, a special lightweight glove was used to as-sist them in doing so. The glove did not contribute to the tan-gential forces.

Secondly, all subjects completed a training period where theypracticed steering under the treatment conditions. Subjects wereasked to maintain their simulated vehicle icon, identified by awhite spot, superimposed on the target track, which appearedto the right of their icon. They were asked to track the line withthe target while steering the 15-s RT, ST, and LT segments of thetrack. The experimental trials began when subjects understoodthe steering tasks. Successful completion of a steering task oc-curred when subjects were able to complete the task without

JOHNSON et al.: EXPERIMENTAL RESULTS USING FORCE-FEEDBACK CUEING IN ROBOT-ASSISTED STROKE THERAPY 339

crashing and stopping the data collection. All subjects had tomeet this minimum measure of task success. A Latin-square de-sign randomized the presentation of the steering tasks [31], [32].

Prior to each steering task, subjects were instructed on howto use their arms (e.g., bi or WA). In bilateral steering underthe force-cue condition, they were advised to grasp the wheelfirmly with both limbs and were instructed to refrain from at-tempting to overpower any forces cues they experienced. In bi-lateral steering under the no-force-cue condition, they were ad-vised to steer with both WA and SA.

A total of four trials were completed for each steering task.The first trial was used as an extended training and only the finalthree trials were used as data. The muscle activity of the WA armwas monitored. A video record was made of each session.

The experimenter’s computer collected torque data, steeringangle position, and calculated steering angle velocity at 300Hz. The STI computer also collected steering angle position(at the slower rate of 10 Hz); these data were used by the STIsystem to calculate vehicle curvature, lateral position, velocity,and acceleration.

The data were examined for the following four conditions:

1) bilateral steering in no force-cue mode (N-bi);2) bilateral steering in force-cue mode (A-bi);3) unilateral impaired or nondominant limb steering in no

force-cue mode (N-WA);4) unilateral impaired or nondominant limb steering in

force-cue mode (A-WA).

Stanford University’s Institutional Review Board approved ourhuman subjects protocol. All subjects signed the informed con-sent form.

3) Data Acquisition and Analysis: For all subjects, the datafor the four steering tasks, N-bi, A-bi, N-WA, and A-WA, wereprocessed and used to evaluate the effect of the corrective forcecues on WA’s force production and muscle activation. Since WAwas in sole control during unilateral steering (N-WA and A-WA)or ( and ), the data sets in these tasks were used toapproximate the maximum force effort of WA, as well as pro-vide a reference muscle activation level for WA during the pre-view-tracking task. The WA unilateral steering data were usedto normalize the WA bilateral steering data for the force-cue andno force-cue conditions. For each data set, the normalized aver-ages were calculated for the steady-state tracking portions (themiddle 9 s) of the RT and LT segments of the preview-trackingtask. In these segments, WA moved either against gravity (a/g),i.e., the wheel was rotated contralaterally so that WA crossed themidsagittal plane of the subject’s body, or with gravity (w/g),i.e., the wheel was rotated ipsilaterally so that WA did not crossthe midsagittal plane of the subject’s body.

Fig. 2 illustrates how the wheel’s movements translated intoWA movement for hemiplegic subjects and control subjects (seeTables II and III). Since the direction in which WA moved couldaffect the muscle activation [22]–[24] and postural adjustments[25], the data were divided by subtasks. The normalized datawere evaluated by subject groups, hemiplegic subjects (Hs)versus control subjects (Ns), and by movement groups, againstgravity and with gravity. Table V shows how the normalizeddata sets for hemiplegic subjects (LHs and RHs) and control

Fig. 2. Wheel’s movement and subtask map to the subjects tested (LNs/LHsand RNs/RHs). WA of left hemiplegics (LHs) and left-controls (LNs) moveagainst gravity in the RT subtask and with gravity in the LT subtask. WA ofright hemiplegics (RHs) and right-controls (RNs) move against gravity in theLT subtask and with gravity in the RT subtask.

TABLE VSUBJECT GROUPING USED IN STATISTICAL TESTS

Hs and Ns were grouped according to with gravity and againstgravity movements. For example, the data for WA of left hemi-plegics (LHs) moving against gravity in the RT subtask weregrouped with the WA of right hemiplegics (RHs) moving againstgravity in the LT subtask. Note that “j” tracks the number ofsubjects.

subjects (LNs and RNs) in the RT ( ) and LT ( )subtasks were combined. The following presents the data nor-malization process. Note that the subscript ( ) refers to the trialnumber while the superscripts are as follows: ( )refers to the four steering tasks, and ( ) refers tothe subjects (Tables II and III).

WA Torque Activity Normalization: From each trial, thetangential forces of weak arm ( ) and strong arm ( )were multiplied by the wheel radius ( ) and averaged at eachtime point across the trials to produce, respectively, an averagelimb torque of

where

(1)and

where (2)

The mean value of the resulting WA and SA average torquesfrom (2) and (3) were calculated for the middle 9 s of the RT( ) and LT ( ) subtasks of each steering tasks.Each subject’s WA average torques, generated during bilateralsteering tasks ( , 2) for the subtasks, were normalized withtheir average WA unilateral torques ( , 4) using

(3)

340 IEEE TRANSACTIONS ON NEURAL SYSTEMS AND REHABILITATION ENGINEERING, VOL. 13, NO. 3, SEPTEMBER 2005

The normalized torque data for each subject, ,provided the percent change in torque production by WAduring bilateral steering with respect to unilateral steering.This measure quantifies how much of the load a subject’s WAassumed during shared steering with respect to its load when itwas wholly responsible for steering. The total difference, ,between the WA’s normalized torque levels for bilateral steeringin the force-cue condition and the no force-cue condition canbe expressed for Hs and Ns using the following relationship:

(4)

A positive percent change indicates that WA’s participationincreased as a result of the force cues.

4) WA EMG Activity Normalization: The sEMG signalswere processed using standard guidelines for collecting, an-alyzing, and reporting of EMG data [33]. A Nicolet VickingII/IIe Electrodiagnostic System collected and processed thesEMG signals. The signals from the Nicolet were then amplified(Gain ), rectified and passed through a low pass filterwith a 20-ms time constant (50 Hz). The partially smoothedsignals were finally sampled in real-time at 100 Hz. The signalswere displayed before and after they were collected. Theywere monitored for faulty electrodes and other artifacts such asexcess noise. Next, all the added gains were removed from thecollected sEMG’s, the data were then filtered using a low-passsecond-order Butterworth filter with 10-Hz cutoff frequency.

Resting sEMG data were collected before the start of the ex-periment. For resting sEMG, subjects were asked to place theWA in their lap in a position such that minimum to no muscleactivity was detected and displayed on the Nicolet. Unilateralsteering with the SA in the no force-cue condition (N-SA) whilethe WA remained relaxed in the lap was used as another mea-sure of minimal WA muscle activity. This measure was used todetermine on/off activation levels for each muscle.

Averaging over three 45-s trials, a subject’s WA averagemuscle activation signal, , for each of the seven muscleswas determined using,

(5)

The muscle activity levels achieved by each muscle in unilat-eral steering, and , were taken as the referencevoluntary contraction for each muscle and used to normalizethe related bilateral data. The normalized muscle activity repre-sents the percent change in a subject’s WA activation levels forthat muscle in the bilateral steering with respect to the unilat-eral steering modes. The percent muscle activity above restingwas determined by subtracting the corresponding normalizedresting levels recorded for WA during unilateral steering withSA, N-SA. Equation (6)

(6)

5) Statistical Analysis: StatView software (SAS instituteInc.) was used for all statistical analysis. Repeated measureand other multifactor ANOVA’s analyses were completed onthe normalized bilateral data according to the subject groupingin Table V [31], [32]. These analyzes assessed the significance

Fig. 3. Average raw torque data of the LNS, LHs, RHs, and RNs in the forceand no force-cue conditions. Data were calculated from the tangential forcesmeasured at the wheel rim for the SA and WA. Graphs show the torques forthe 45-s driving interval with an example of the steady-state portions used forright and left turn analysis (Table V). WA torques changed significantly acrossmodes.

of main interaction effects of subject grouping, movementdirection, and force-cue condition on the dependent variables.Post-Hoc analysis was performed using Tukey–Kramer statistictests. Although the number of subjects was small, the data werenormally distributed.

IV. RESULTS

A. WA Torque Activity

Fig. 3 shows SA and WA torque averages for RHs, RNs,LHs, and LNs across the 45-s driving interval for the forceand no force-cue conditions. The boxed portion identifies thesteady-state portions analyzed in this paper. The normalizedtorques for each subject is shown in Fig. 4. For the most part,individual torque profiles followed the trends seen in this figure.Individual profiles were consistent in that they fluctuated abouta clear average so each person’s average profile was represen-tative of their movements. Fig. 4(a)–(d) shows four plots com-paring the normalized torques ( ) produced by sub-ject’s WA during the force-cue (A-bi: ) condition with theno force-cue (N-bi: ) condition in the bilateral steering.Grouped according to with-gravity (w/g) and against-gravity(a/g) movements, Fig. 4(a) and (b) shows the normalized torquesfor the WA of hemiplegic subjects (Hs) grouped according toTable V. Fig. 4(c) and (d) show the corresponding graphs forcontrol subjects (Ns) in the w/g and a/g movements. A value of100% means that WA was equally active in both unilateral andbilateral steering; a smaller positive value means that WA par-ticipated less during bilateral steering while a zero value meansthat WA was not being used to generate torque during bilat-eral steering. A negative percent torque means that the directionof WA’s torques during bilateral steering opposed its directionduring unilateral steering, i.e., the WA did not do work in theappropriate movement direction (see Fig. 2 for WA’s desired

JOHNSON et al.: EXPERIMENTAL RESULTS USING FORCE-FEEDBACK CUEING IN ROBOT-ASSISTED STROKE THERAPY 341

Fig. 4. Comparison of the normalized torques for WA movements during bilateral steering. Normalized torque of 100% indicates that the WA torque level was atthe same magnitude and in the same direction as during unilateral steering. Movements shown are for the force-cue (A-bi) condition with the no force-cue (N-bi)condition for subjects (Table V). Key points are as follows. In the with-gravity movement, WA torques for both Hs and Ns during bilateral steering in A-bi were notsignificantly different from the N-bi ones. WA actively participated in both force conditions. In the against-gravity movement, WA torques during bilateral steeringin A-bi were significantly different from the N-bi ones for both Hs and Ns. However, the significant differences were significantly greater for Hs. For several Hs(LH1, LH3, LH4, RH1, and RH4) in the no force-cue condition, the WA contributed torques opposed the direction of intended movement.

movement direction). Fig. 4(b) shows that in a/g movementsand no force-cue condition, several hemiplegic subjects (e.g.,LH1, LH3, LH4, and RH1) produced large negative torqueswith WA. The torques were counter-productive to the task in-dicating that the WA tangential force production was oppositeto the desired movement direction. The force cues reduced thenegative torques and increased the WA torque activity in the ap-propriate directions. ct subjects having minimal to no impair-ment (stage V).

The results of repeated measure analysis (see Table VI)revealed significant differences between subject groups (Nsversus Hs) ( ), between movement directions (w/gand a/g) ( ) and between the force-cue conditions(force-cue versus no force-cue) ( ). A significant in-teraction was found between movement direction and force-cueconditions ( ), indicating that differences in WA’storques activity for Ns and Hs depended on the movementdirection.

Given the interaction effects, the means between the differentgroups in the movement directions were examined. Fig. 5 graph-ically shows the means of the WA torque activity for Ns andHs subject by movement directions and force-cue condition. Wecan reliably conclude that there were significant differences inwhat subjects did in the force-cue and no force-cue modes onlyin the against gravity movement.

Fig. 6 summarizes a two-factor ANOVA comparing the per-cent change in the torque produced ( ) by WA of both Nsand Hs during bilateral steering as a result of the force cuesfor with-gravity and against-gravity movements. It was hypoth-esized that the presence of force cues would cause subjects’WA torque activity in the direction appropriate to the steeringtask to significantly increase. Fig. 6 shows that for both Ns andHs, the percent change in torque produced by their WA duringthe against-gravity movement was significantly more with forcecues than without. Positive changes indicated increased WAparticipation in the steering task. On average, the presence of

342 IEEE TRANSACTIONS ON NEURAL SYSTEMS AND REHABILITATION ENGINEERING, VOL. 13, NO. 3, SEPTEMBER 2005

TABLE VISUMMARY OF REPEATED MEASURES ANALYSIS RESULTS ON THE PERCENT WA

TORQUE ACTIVITY AND PERCENT EMG ACTIVITY

Results show that there were significant changes in WA Torque ac-tivity between the two treatment conditions for Ns and Hs in w/g anda/g movements.

Fig. 5. Interaction bar plot for the WA Torques for Ns and Hs by movementdirection and force-cue modes. From these plots, it is clear that the differencesin the WA torque activity were dependent on the movement direction.

Fig. 6. Interaction plot comparing the percent change in torque produced byNs’ WA and Hs’ WA during the bimanual steering as a result of the force cues.

force cues in a/g caused Ns’ WA torque effort to positively in-crease by 63% ( ) and Hs’ WA torque effort to pos-itively increase by 153% ( ). On the other hand, inwith-gravity movement, the presence of force cues only causedinsignificant changes in percent torque produced by Ns’ WA (in-creased by 18%: ) and Hs’ WA (increased by 17%:

). The fact that the force cues did not have a signifi-cant effect on WA’s torque production in the with-gravity move-ment was an unexpected result.

Since Ns had no tendencies toward overuse of their SA, wehypothesized that the impact of force cues on the productivetorque effort of WA would be greater for Hs than for Ns. Fig. 6illustrates that the force cues had a greater impact on the WAof hemiplegic subjects in the against-gravity movement. Re-sults confirm that the presence of force cues had a significantlygreater effect on the torque activity of the WA of hemiplegicsubjects than on the WA of control subjects ( ).

B. WA Muscle Activity

Fig. 7 illustrates the data averages of normalized sEMGs (thepercent muscle activity above resting) in the against gravitymovement for the measured muscles (Pt, Traps, Mdel, Tri, Bi)of LNs and LHs under the two force-cue conditions. For sev-eral subjects, sEMG data for the Lats, the Pecs, or the Trapsor some combination thereof was contaminated by electrocar-diogram (ECG) activity. Therefore, contaminated data were ex-cluded from the statistical analysis.

It was hypothesized that increases in the weak arm’s sEMGsactivity levels would correspond to increases in WA force effortdue to the force-cue condition. It was unclear which muscleswould significantly increase in activity. The repeated measureanalysis (see Table VI) revealed significant differences betweenmovement directions (w/g and a/g) ( ) and be-tween the force-cue conditions (force-cue versus no force-cue)( ). Significant interactions were found betweenforce conditions and the movement direction ( ) andbetween the muscles and the movement direction ( ).These interactions indicated that increases in sEMG magni-tudes due to the force cues were inconsistent. It depended onmovement directions and on individual muscles. To investigatefurther, we tested for significant differences by comparing,within each muscle type, the muscle activation achieved in thetwo conditions for Hs and Ns in a/g and w/g movements. Asignificant result indicated that, for a given number of subjects( ), the muscle being evaluated increased its percent activityduring bilateral steering in the force-cue condition withinthe against-gravity or with-gravity movement. For the WA ofhemiplegic subjects, three muscles (Pecs, Mdel, and Bi) werefound to change significantly when force cues were presentduring bilateral steering in the a/g movement. The triceps andthe pronator teres muscles were borderline in that the confi-dence interval was approximately 94%. The force cues had nosignificant impact on WA muscle activation levels for Hs inthe w/g movement or for Ns in either a/g or w/g movement.Table VII summarizes the normalized mean activation levelsfor WA muscles for Hs and Ns.

Fig. 8 summarizes the observed percent ( ) changes inmuscle activation levels as a result of the force cue for all sevenmuscles for Ns and Hs. The table directly below the figure re-ports the mean differences. Results show changes due to forcecues in w/g and a/g movement: (a) interaction plot for Ns’ WAmuscles and (b) interaction plot for Hs’ WA muscles. On av-erage, the increase in the activity levels for the Mdel and Bi

JOHNSON et al.: EXPERIMENTAL RESULTS USING FORCE-FEEDBACK CUEING IN ROBOT-ASSISTED STROKE THERAPY 343

Fig. 7. Graphical examples of the sEMG data from which the mean difference values in Fig. 8 were derived. Graphs show normalized WA sEMGs for Ns andLHs in the against-gravity movement. Percent sEMGs are calculated using (6). No force-cue condition is the lighter shaded region while the darker shaded regionrepresents the force-cue condition. First row of graphs show combined percent sEMGs for the left control subjects. Top-row of plots averages of the sEMGs forall LNs. Remaining plots show average plots for subjects LH1-LH4. For example, the figure illustrates how some hemiplegic subjects (e.g., LH3) had abnormalsEMGs activity levels in Pt and Bi as compared to the LNs.

muscles of the Hs WA’s ranged from 20% to 28%. The averageincrease in the Pecs muscle of Hs ( ) WA’s was 33.8%.

C. Postural Activity

An occupational therapist (OT) reviewed the video records,which showed the gross movement of the trunk and shouldersduring the steering tasks. Table VIII summarizes the Occu-pational Therapist’s (OT) assessment of hemiplegic subjects’postural movements during the steering tasks [33]. The OTconcluded that the movements of LH1, LH4, and RH4 wereexcessive and, therefore, may have influenced impaired armmuscle activity. Excessive movements (E) occurred when theshoulder targets moved outside an area (1.0 cm 1.0 cm)during steering movement. LH1 had a balance problem thatcaused her to elevate her shoulders and lean out of the normalregion during the right turns. LH4 tended to lean forwardslightly and elevate his shoulders during right turns, but onlyfor unilateral steering. RH4 tended to elevate his shouldersduring left turns of the bilateral steering trials. For both LH4and RH4, these movements were of the against-gravity type. Ingeneral, the postural movements that occurred were primarilyleft and right leaning of the trunk and shoulder elevation.

The report of the occupational therapist on postural activityobserved in the video data was examined and qualitativelycompared with Hs Brunnstrom’s stage [34] and UE F-M score(Table IX). There are six Brunnstrom stages that determinethe extent of recovery of motor function after stroke. Hemi-plegic subjects in lower Brunnstrom stages exhibit synergisticmovement patterns. Stage I is the flaccid stage and Stage VIis the isolated movement stage. Subject RH4 was severelyimpaired (stage II). Three subjects (LH3, LH4, and RH1) were

moderately impaired (stages III), one mildly impaired (stageIV), and three were like neurologically inta

Hemiplegic subjects in low functioning stages, especiallystages II and III, also exhibited flexor synergy as reflectedby the UE F-M flexor synergy sub-score. All three subjectswith abnormal postural behaviors (LH1, LH4, and RH4) hadsome flexor synergy. Only two were low functioning subjectsaccording to the UE F-M scores. These subjects also had diffi-culty in the no force-cue condition and had the most difficultyusing their impaired arm during the steering task in this mode(Fig. 4).

It was believed that abnormal postural behavior would notbe wholly responsible for increases observed in the related WAtorque activity. This hypothesis was analyzed qualitatively. Forsubjects observed to use abnormal postural movements, thesEMG data was examined for above-resting level activity inmuscles that were not directly influenced by trunk movementssuch as the middle deltoid, triceps, and biceps. These threemuscles were active (sEMG’s level above resting levels) whensubjects with abnormal postural movements were engagedin the steering task during the force-cue condition. Of thethree muscles, the middle deltoid and the bicep muscles weresignificantly different across force-cue conditions.

V. DISCUSSION

Corrective force cues had some effect on the WA participa-tion rate (as characterized by productive torque activity) of allsubjects during bilateral steering of our preview-tracking task.The force cue effect was only significant in subtasks that re-quired subjects to move the wheel contralaterally, which causedtheir WA to move toward their SA side and against gravity. The

344 IEEE TRANSACTIONS ON NEURAL SYSTEMS AND REHABILITATION ENGINEERING, VOL. 13, NO. 3, SEPTEMBER 2005

TABLE VIISUMMARY OF SIGNIFICANT TEST RESULTS ON THE PERCENT MUSCLE ACTIVITY ACROSS MODES

Results show that there were significant increases in muscle activity due to force cues for Hs in a/g movementsonly. S: significant p < 0:05 and NS: not significant. Number of subjects included in the analysis is indicatedby “n.” The sEMG data for the Traps were usable for all but one control subject. Data for the Pecs was usablefor 11 subjects (5 Ns and 6 Hs); the data for the Lats were usable for nine subjects (5 Ns and 4 Hs). Traps andLats were not significant for all subjects. Pronator Teres and Triceps were borderline significant for Hs in a/gdirection p = 0:06.

fact that force cues did not have a significant effect on H’s WA’sparticipation in both movements was an unexpected result.

The presence of directionally inappropriate torques in the noforce-cue mode could be attributed to handedness or the pres-ence of maladaptive behavior. In the case of hemiplegic sub-jects, this behavior could be attributed to learned nonuse ten-dencies or their motor impairment level. Fig. 4(b) showed thatin normal bilateral steering without force cues, hemiplegic sub-jects had a difficult time moving their weaker, impaired armagainst gravity (medially, toward their less-affected side). Theirdifficulty was further amplified if they had a motor impairmentthat affected their ability to independently control their muscles,as assessed by their Fugl–Meyer score and Brunnstrom stage(Table VIII), i.e., if they had some synergistic and patternedmovements (stages II, III, and IV). For example, according toFig. 4(b), right hemiplegic subjects had trouble in the left turnsubtask (the a/g movement). If, like RH1 and RH4, they hadhigher levels of motor impairment (a low UE F-M score) in theirlimb (or higher learned nonuse behavior), their impaired arm ef-fort was negative. This suggests that their WA was hindering thetask in the no force-cue condition.

In bilateral steering with no force cues, RH1’s and RH4’sWA dragged on the wheel and did not positively contribute tothe steering task. In other words, the torque activity of the WAmoved the wheel in a direction opposite to the direction requiredin the LT subtask. When the force cues were introduced in theA-bi force-cue condition, RH1’s and RH4’s impaired arm sig-nificantly increased its torque production. Their WA contributed

more to the task. Fig. 4(b) also indicates that the impaired arm ofLH1, LH3, and LH4 in the RT (their a/g movement) functionedsimilarly to the WA of RH1 and RH4, however, for LH3 andLH4, the force cues appeared to assist them to increase their im-paired torque effort in the direction appropriate for the steeringtask. LH3 and LH4 were not able to get their WA to contributepositively to the task because they were unable to not overusetheir SA. They only partially obeyed the force cues. The WAof LH2, RH2, and RH3 appears to function like the WA of Nsunder the force-cue condition. This result could have been dueto their higher level of motor function as indicated by their UEF-M scores.

In summary, the force cue appeared to be able to counteractthe tendency for WA to produce counter-productive torques inthe a/g movement direction. Therefore, the presence of the forcecues had some effect on assisting the WA to contribute moreto the steering task. The impact of the force cues on WA ofHs in a/g movements was supported by the sEMG data. ThesEMG data (Table VI) indicated that increases in the impairedarms’ torque effort in the A-bi force-cue condition was accom-panied by significant increases in the muscle activity for three ofseven muscles monitored in Hs. Video revealed that three hemi-plegic subjects had some excessive postural activity during bi-lateral steering, but the postural movements did not appear tobe the main mechanism these subjects used to complete theiragainst-gravity movements. The percent changes in the sEMGdata (Fig. 8) confirm that the significant increases in WA torqueswere likely due to increased use of muscles important to the

JOHNSON et al.: EXPERIMENTAL RESULTS USING FORCE-FEEDBACK CUEING IN ROBOT-ASSISTED STROKE THERAPY 345

Fig. 8. Summary of the percent change in muscle activation levels for seven muscles of WA for all subjects. Mean differences between the two modes arereported. Results show changes due to force cues in w/g and a/g movement. (a) Interaction plot for Ns’ WA muscles. (b) Interaction plot for Hs’ WA muscles.Figure graphically illustrates that within each muscle type, Hs’ WA muscle activation due to the force cues was typically higher in against-gravity than with-gravitymovement. Middle 9 s of the RT and LT subtasks were used to calculated the average normalized sEMGS in the RT and LT, k � k and k � k, respectively.The fact that both the triceps and the biceps increased activity suggests co-activation.

TABLE VIIISUMMARY OF SIGNIFICANT RESULTS FOR POSTURAL ACTIVITY

Results show the Occupation Therapist’s assessment of hemiplegic subjectsfor abnormal postural adjustments. E: excessive and NE: not excessive.Excessive movement was defined as occurring when the shoulder targetsmoved outside an area (1� 1 cm ) during steering movement.

tracking task such as the middle deltoid, the triceps, and the bi-ceps [22], [23]. Increases in muscle activation levels for both thetriceps and biceps suggest co-activation of these muscles.

Control subjects also increased their nondominant limb’seffort in against-gravity movements. However, in normalsteering without force cues, their nondominant limb was lesslikely to hinder the task, unlike most of our hemiplegic subjects’impaired arm activity. When the force cue was introduced, therewas also significant increase in Ns’ nondominant limb torqueproduction. However, the effect of the force cues on theirnondominant limb was shown to be not as large as for Hs’impaired arm.

The force cues had no significant impact on the muscle ac-tivation levels of the seven muscles monitored for control sub-jects’ WA. The WA muscle activities of control subjects ap-peared to be the same across the force-cue and no force-cueconditions. This may be because control subjects typically useboth WA and SA. Control subjects tended to use their WA asmuch as the SA in the bilateral steering tasks without forcecues (N-bi) and when the force cues were introduced theywere able to obey the force cues, i.e., not use their SA, butuse their WA to steer instead. This finding further supportsthe result that the force cues had a greater overall effect onthe impaired arm of hemiplegic subjects than on the nondom-inant limb of control subjects.

346 IEEE TRANSACTIONS ON NEURAL SYSTEMS AND REHABILITATION ENGINEERING, VOL. 13, NO. 3, SEPTEMBER 2005

TABLE IXCOMPARISON OF MUSCLE AND POSTURAL ACTIVITY RESULTS WITH FUNCTIONAL ASSESSMENT SCORES

Table compares OT’s assessment of hemiplegic subjects for abnormal postural adjustments (E: excessive and NE: notexcessive) with motor function levels on UE F-M and Brunnstrom stages. UE F-M scores were converted to theirequivalent Brunnstrom stages.

The force cues effect depended on movement direction. Thisstrong correlation to steering movements against gravity wasunexpected. Several explanations are suggested. The bias re-sult could be interpreted from a biomechanical perspective sincesteering movements against gravity required higher muscle ac-tivation levels as well as more muscle coordination [21], [25].Alternatively, the force cues dependence on steering directionmay have been due to how our tracking task was designed. Thetracking task was not randomly presented to the subject; it re-quired relatively slow and steady tracking movement, and sub-jects were required to steer only one combination of w/g anda/g. The predictable and relatively slow tracking tasks may haveinfluenced the significant interaction with the biomechanicallymore difficult a/g movements. If subjects were presented witha random tracking task that required faster movement timesmaking it equally challenging to do a/g and w/g movements,the study design bias toward a/g movements would be removed.With this challenge, a better determination could then be madeas to whether the corrective force cues can have a significant in-crease in WA activity of hemiplegic subjects in both movementdirections. If it can be shown that force cues can significantlyaid the impaired arm in both w/g and a/g movements, then astronger case can be made for the potential benefits of correc-tive force cues.

The aim of this study was to assess the potential of correc-tive force cues to decrease overuse of the less-affected arm in atwo-handed task by increasing the level of involvement of theimpaired arm. In this study, we saw a significant force cue ef-fect on the impaired arm of hemiplegic subjects during partic-ular movements in one therapy session with the driver’s SEAT,indicating that hemiplegic subjects used their impaired arm dif-ferently in each of the force-cue condition. One possible expla-nation for this could be in differing interpretations of the steeringinstruction. The instruction to relax and not fight the force cuecould have been interpreted by some subjects to not use the SAarm and only use the WA arm. Although a source of error, wesuggest this was not the most likely explanation for the changesin the use of the WA. All subjects did use their strong arm inboth conditions. The data support the fact that the force-cue ef-

fect became significant when the demand for the WA increased.In other words, it appeared that when the ability in their im-paired arm was not sufficient to accomplish task (e.g., completeout-of-flexor synergy movements), hemiplegic persons tendedto produce torques with the impaired arm that were counter-pro-ductive to the desired steering direction. The presence of theforce cues caused significant changes in the use of the impairedarm. Although some hemiplegic subjects never saw a positivetorque contribution out of their WA, they significantly increaseduse of the limb in the productive direction.

Since maladaptive behavior is typically not an issue with con-trol subjects, the difference in the use of the impaired arm in theforce-cue and no force-cue modes for control subjects shouldhave been insignificant. Counter-productive torques were seenfor left-handed control subjects, which suggest that dominancemay play a role in interpreting the results and the additional needfor caution in making generalization of these result [Fig. 4(d)].

Results appear to agree with observations by Brunnstrom [34]that if hemiplegic subjects are in a motor impairment recoverystage where synergistic movement patterns predominate, theymay resist arm movements in directions contrary to these syn-ergy patterns. Since according to Brunnstrom and Bobath [35],the predominant synergic pattern in the upper limb is the flexorpattern, it is not surprising that hemiplegic subjects were lessable to use their WA during movements against the flexor pat-tern. In terms of steering, this will most likely be during contra-lateral rotations of the wheel or against gravity movement of theimpaired arm.

The heterogeneity of the stroke population and our smallsample size make it hard to generalize the observed effect ofthe corrective force cues on the activity of the WA. The factthat force cues had significant effect on increasing productiveWA torque activity in movements against gravity still suggestsa potential value of corrective force cues as a device-basedtherapy method to help hemiplegic subjects become aware oftheir overuse of the less-affected limb. The results here supportthe potential usefulness of this mode as a restraint-type trainingtool to encourage increased use of the impaired arm in the faceof overuse of the less-affected arm.

JOHNSON et al.: EXPERIMENTAL RESULTS USING FORCE-FEEDBACK CUEING IN ROBOT-ASSISTED STROKE THERAPY 347

VI. CONCLUSION

In this study, we saw a significant force cue effect on the im-paired arm of hemiplegic subjects during particular movementsin one therapy session with the driver’s SEAT. The presence ofthe force cues had some effect on assisting the WA to contributemore to the steering task. The force-cue mode effect was direc-tion dependent; the force-cue action was able to counteract thetendency for the impaired arm of hemiplegic subjects to producecounter-productive torques during bilateral steering in steeringsegments requiring impaired arm movements up and againstgravity. For the against-gravity movement of the WA, the in-creases in the productive torque activity of the hemiplegic sub-jects’ weaker impaired arm were significantly greater than in-creases observed in control subjects’ weaker nondominant limb.An accompanying significant increase in EMG activity for sev-eral muscles of the impaired arm was also observed.

This pilot study did not address the long-term effect of theforce-cue on the impaired arm use of hemiplegic subjects or car-ryover of training on driver’s SEAT in this mode. These resultsgive us confidence to further study the parameters governing theeffectiveness of this type of force-cueing. Further study is alsoneeded to assess whether a longer training period on driver’sSEAT, where this compensatory awareness is combined withmass-practice, could result in increased use of the impaired limbin steering-like tasks or real-world tasks requiring similar move-ment primitives such as those where the arm moves mediallyacross the sagittal plane.

ACKNOWLEDGMENT

The authors would like to thank their colleagues at the Vet-erans Affairs Research and Development Center, Palo Alto, CA,especially Dr. P. Lum (now with Virginia Commonwealth Uni-versity, Richmond), D. Jaffe, Dr. C. Patten, and D. Kenney.

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348 IEEE TRANSACTIONS ON NEURAL SYSTEMS AND REHABILITATION ENGINEERING, VOL. 13, NO. 3, SEPTEMBER 2005

Michelle J. Johnson (M’02) received the B.S. de-gree in mechanical engineering from the Universityof Pennsylvania, Philadelphia, in 1990, the M.S.degree in mechanical engineering with an emphasison robotics from the University of California, Irvine,in 1994, and the Ph.D. degree in mechanical engi-neering with an emphasis on mechatronics, robotics,and design from Stanford University, Stanford, CA,in 2001.

She completed a postdoctoral fellowship at theAdvanced Robotics Technology and Systems Lab-

oratory, Scuola Superiore Sant’Anna, Pisa, Italy, in 2003. She is currently anAssistant Professor in the Department of Physical Medicine and Rehabilitation,Medical College of Wisconsin, Milwaukee, and a Research Assistant Professorin the Department of Biomedical Engineering at Marquette University, Mil-waukee, WI. Her research interests focus on robotic applications to functionalrehabilitation and on improving methods for design and development of roboticand mechatronic technology for rehabilitative and assisted living environments.

H. F. Machiel Van der Loos (M’95) received theIngénieur Mécanicien degree from the Swiss FederalInstitute of Technology, Lausanne, Switzerland, in1979, and the Engineer’s Degree in 1984 and thePh.D. degree in 1992 from Stanford University,Stanford, CA, in mechanical engineering, all inrobotics.

He is Co-Principal Investigator on several feder-ally funded mechatronics projects at the Palo AltoVeterans Administration Rehabilitation Research andDevelopment Center, Palo Alto, CA. These projects

explore assistance and therapy applications of robotics for persons who havedisabilities as a result of SCI and stroke. He is a Consulting Associate Professorwith the Department of Functional Restoration, Stanford University.

Dr. Van der Loos is an Associate Editor of the IEEE TRANSACTIONS ON

NEURAL SYSTEMS AND REHABILITATION ENGINEERING.

Charles G. Burgar (S’72–M’75) received the B.S.degree in electrical engineering from the Universityof Texas, Austin, in 1974, and the M.D. degree fromthe University of Texas Health Science Center, SanAntonio, in 1984.

He is Co-Principal Investigator on several feder-ally funded projects at the Palo Alto Veterans Admin-istration Rehabilitation Research and DevelopmentCenter, Palo Alto, CA. These projects explore robot-assisted neurorehabilitation following stroke. His re-search interests are in physical medicine and rehabil-

itation and electrodiagnosis of neuromuscular diseases. He is the Medical Di-rector of the Palo Alto Veterans Administration Rehabilitation Research andDevelopment Center and a Clinical Assistant Professor with the Department ofFunctional Restoration, Stanford University, Stanford, CA.

Peggy Shor received the B.S. degree in occupationaltherapy from San Jose State University, San Jose, CA,in 1988.

She is a Research Occupational Therapist workingon several projects focused on exploring robot-as-sisted neurorehabilitation at the Palo Alto VeteransAdministration Rehabilitation Research and De-velopment Center, Palo Alto, CA. Her researchinterests are human services and robotic rehabil-itation, functional restoration and rehabilitation,and effectiveness of neurodevelopment treatment

techniques for persons with adult hemiplegia.

Larry J. Leifer (M’69) received the B.S. degreein general engineering science, the M.S. degree inproduct design, and the Ph.D. degree in biomedicalengineering from Stanford University, Stanford, CA,in 1962, 1963, and 1969, respectively.

He is a Professor of Mechanical Engineering De-sign and Founding Director of the Stanford Centerfor Design Research (since 1982). He has publishedin the areas of diagnostic electro-physiology, func-tional assessment of voluntary movement, humanoperator information processing, rehabilitation

robotics, design team protocol analysis, design knowledge management, andconcurrent engineering. As a Member of the Stanford Faculty since 1976, hehas taught product design, created the smart product design (mechatronics)curriculum at Stanford, and most recently, teaches a graduate course in“Team-Based Design Innovation with Corporate Partners.” He was FoundingDirector of the Stanford-Palo Alto Veterans Administration RehabilitationResearch and Development Center (1978–1989), and more recently, FoundingDirector of the Stanford University Learning Laboratory (1997–2001). Withthe intent to disseminate orphaned medical device technology, he co-foundedLingraphicare America (1989) and Independence Works (1992).