Archives of Physical Medicine and Rehabilitation
Volume 90, Issue 2 , Pages 263-270, February 2009

Improvement of Gaze Control After Balance and Eye Movement Training in Patients With Progressive Supranuclear Palsy: A Quasi-Randomized Controlled Trial

Department of Physical Medicine and Rehabilitation, University of Minnesota, Minneapolis, MN

Article Outline

Abstract 

Zampieri C, Di Fabio RP. Improvement of gaze control after balance and eye movement training in patients with progressive supranuclear palsy: a quasi-randomized controlled trial.

Objective

One of the main oculomotor findings in progressive supranuclear palsy (PSP) is the inability to saccade downward. In addition, people with PSP have difficulty suppressing fixation, which may contribute to vertical gaze palsy. The objective was to investigate the effectiveness of a rehabilitation intervention tailored to enhance suppression of fixation and gaze shift in participants with PSP.

Design

Controlled trial with a quasi-randomized design. Measures occurred at week 1 and 5. Researchers assessing participants were blind to the group assignments.

Setting

Movement disorders assessment laboratory.

Participants

Nineteen adults with possible or probable PSP who were ambulatory for short distances and had far visual acuity of 20/80 and a Folstein Mini-Mental State score of more than 23.

Interventions

Balance training complemented with eye movement and visual awareness exercises was compared with balance training alone.

Main Outcome Measures

Gaze control was assessed using a vertical Gaze Fixation Score and a Gaze Error Index.

Results

Gaze control after the balance plus eye exercise significantly improved, whereas no significant improvement was observed for the group that received balance training alone.

Conclusions

These preliminary findings support the use of balance and eye movement exercises to improve gaze control in PSP.

Key Words: Eye movements, Rehabilitation, Supranuclear palsy, progressive, Reflex, vestibulo-ocular

List of Abbreviations: ANOVA, analysis of variance, FEF, frontal eye field, PD, Parkinson disease, PSP, progressive supranuclear palsy, RMS, root-mean-square, UPDRS, Unified Parkinson Disease Rating Scale, VOR, vestibuloocular reflex

 

PROGRESSIVE SUPRANUCLEAR PALSY is a parkinsonian syndrome that typically affects gait and oculomotor control.1, 2, 3 One of the main oculomotor findings in PSP is the inability to saccade downward, which is referred to as vertical gaze palsy.1, 2, 3 Slow saccades in the vertical direction or complete gaze palsy are some of the criteria for the clinical diagnosis of PSP.4

Although patients with PSP have impaired ability to shift gaze downward, their ability to fixate on objects in the environment while their heads move is grossly intact.5 Fixation ability is derived from the VOR, which is not affected by supranuclear pathology. During our daily life activities, the VOR is important because it provides a mechanism to stabilize gaze by holding fixation on points of interest in the environment. In order to shift gaze to objects of interest, however, the VOR must be suppressed.6, 7

It is known that people with PSP have difficulty suppressing the VOR,5, 8, 9 and this deficit might exacerbate vertical gaze palsy.8 The inability to generate saccades can compromise one's safe ambulation. Anticipatory saccades occur normally in situations that involve changing direction of walking10 or prior to obstacle avoidance.11 When saccades are not generated as often, there is an increase in risk for falling.12

Aside from interfering with locomotion, the inability to suppress the VOR can interfere with cognition.13 Deficits in cognition, especially attention and executive function, have also been linked to an increased risk for falling in the elderly,14 in Alzheimer disease,15 and in PD.16 In PSP, particularly, a strong correlation has been found between the ability to suppress the vertical VOR and certain domains of cognition: attention and visual awareness.13

Traditional measurements of gaze behavior usually involve the measurement of actual gaze angles to footfall location during obstacle step-over tasks11 and platform tasks.17 Such measurements are assessed along with spatiotemporal locomotor patterns, and the results of these studies show that there is a link between the control of oculomotor function and locomotor function, with the locomotor system controlled in a feed-forward manner by the oculomotor system.

Even though evidence shows that ocular mobility is important in the control of locomotion and cognitive aspects related to awareness, eye movement rehabilitation is often neglected as a therapeutic approach to treat patients with PSP. In the literature, a single case study reports the use of eye-head movement retraining to treat PSP.18

In the present study, we investigated the effectiveness of a rehabilitation intervention tailored to enhance suppression of fixation and gaze shift in a group of participants with PSP. We used an experimental paradigm involving a platform step-up activity to assess gaze control during a functional task. The objective of this study was to determine whether eye movement exercises associated with balance training can improve gaze control in PSP during a platform step-up activity. A study using the same patient sample, but addressing a different research question, reported changes in gait and mobility with the interventions described here. This study is published elsewhere.19

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Methods 

Participants 

Twenty subjects with PSP, living in the community were enrolled in this study. Subjects were recruited through the University of Minnesota Movement Disorders Clinic, local PD clinics, and the PSP Society. Recruitment occurred during a period of 2 years. To be included, subjects needed a diagnosis of a possible or probable PSP according to the criteria established by the National Institute of Neurological Disorders and Stroke.4 Diagnosis was made by a certified neurologist, specialized in movement disorders. In addition, other inclusion criteria were (1) ability to walk short distances independently (with an assistive device if necessary and guarded, but without the direct assistance of another person), (2) Folstein Mini-Mental State Examination score greater than or equal to 23,20 and (3) a corrected far visual acuity of at least 20/80. No changes in medication were implemented for this investigation. Prior to enrollment, subjects came to the University of Minnesota, where they were screened to make sure they met the inclusion criteria. The protocol for this study was approved by the University of Minnesota Human Subjects Research Committee, and all participants provided informed consent prior to enrolling.

Design 

A quasi-randomized controlled trial with partial crossover design was used to study the effects of balance and eye movement training (balance plus eye) compared with balance training alone on gaze control. Twenty subjects were alternately assigned to either a treatment group (balance plus eye) or a comparison group (balance only) with exception for allocation allowed by geographic distance from the testing center (several patients who resided in distant locations and were unable to participate in the crossover component of the study were allocated to the treatment group which did not crossover). In order to validate the allocation procedure, the equivalence of baseline characteristics among control and treatment groups was evaluated (see Results section, Baseline Measurements). The crossover component of the larger study is not presented here. Only the pretest-posttest phase was analyzed for this report. For details on the flow of participants throughout the trial, please see the flow diagram (appendix 1). The study took place during 3 years, from 2002 to 2005.

Baseline and postintervention assessments occurred at week 1 and week 5 and were undertaken by a group of physical therapy students who were blind to group assignments. Baseline characteristics assessed in both groups were (1) diagnosis (possible vs probable), (2) sex (men vs women), (3) age, (4) time of symptom onset, (5) dementia with the Folstein Mini-Mental State Examination Score,20 and (6) severity of symptoms with the UPDRS-motor section21 and PSP rating scale.22 The UPDRS-motor section is used primarily for patients with PD, but more recently it has been tested in PSP, and it has shown high internal consistency, with a Cronbach α=0.90.21 The PSP rating scale is specific for PSP and it has good interrater reliability with an intraclass correlation coefficient of 0.86.22

Assessment of Outcome 

Task 

Participants were asked to step onto a wooden platform and step down on the other side. The platform was 17.5cm in height (57cm width, 48cm depth). At the start of each trial, they were instructed to stand still and look straight ahead (so that a baseline eye signal could be established). They were to start after a command of “go” and were told they could look anywhere to complete the task after that command. Four trials were collected.

Outcome measures 

Two primary outcomes were assessed in this study: (1) the vertical Gaze Fixation Score and (2) the Gaze Error Index.

Vertical gaze fixation score 

Traditional measures of gaze-shift ability use a direct measure of the gaze angle.10, 23, 24 In PSP, however, patients experience difficulty suppressing the VOR to initiate a gaze shift. Therefore, change in gaze angle alone is not sensitive to reflect the relationship between the head and eye movements. A down gaze angle of 20°, for example, could be a result exclusively of head pitch, eye pitch, or a combination of head and eye motion. A sensitive marker of gaze rehabilitation needs to detect the relationship between gaze angle and the relative contributions of head and eye motion.

Di Fabio et al8 developed the vertical Gaze Fixation Score to address this problem. The vertical Gaze Fixation Score is derived from the RMS error of the head pitch versus vertical eye position traces and is then normalized to peak-to-peak gaze amplitude. This score has been used previously to assess VOR suppression in people with PSP while seated13 and also to evaluate gaze shift ability while subjects with PSP initiated platform stepping.8 The vertical Gaze Fixation Score is a measure of eye-head coordination because it relies on RMS error calculation. From the vertical Gaze Fixation Score, we can infer the amount of gaze shift or suppression of fixation as participants step up on a platform.

In theory, the vertical Gaze Fixation Score has a range from 0 (perfect concordance of vertical eye-in-head and head pitch traces with maximal gaze shift) to infinity (perfect gaze stabilization with maximal discordance between head pitch and vertical eye traces). Therefore, a low vertical Gaze Fixation Score indicates suppression of the fixation to prepare for gaze shift, whereas a high vertical Gaze Fixation Score indicates greater fixation. An improvement in our participants means a lower vertical Gaze Fixation Score.

The interval of time during which the vertical Gaze Fixation Score was calculated on the platform task is illustrated in figure 1. The vertical Gaze Fixation Score was calculated starting at onset of downward head pitch and until the point where the lead foot departed from the platform.

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  • Figure 1. 

    Time interval for vGFS and GEI calculation. (A) Foot (z-axis), head pitch, and vertical eye traces during a platform task. Subject started the task standing and looking straight ahead. The vertical Gaze Fixation Score (vGFS) was calculated starting at head pitch until the lag foot departed from the platform (blue arrow). (B) Head pitch velocity for the same trial. The vertical dashed trace indicates peak of head pitch velocity. Actual gaze angle was calculated at the point in time when head pitch velocity peaked down. Abbreviations: deg, degrees; GEI, Gaze Error Index.

Gaze error index 

The Gaze Error Index is a measurement of discrepancy between the participants' actual gaze angle and the gaze angle needed if they were to fixate on the footfall location.8

In order to obtain the Gaze Error Index, we needed to first calculate the actual gaze angle and the gaze to footfall location. We calculated the actual gaze angle in the vertical direction as the sum of head pitch and vertical eye movement at the point in time when the participants' head pitch velocity peaked downward prior to step initiation during the platform step up task (see figure 1).

Predicted gaze angle to footfall location was calculated based on the participants' orbit height and step amplitude onto the platform, applying an inverse tangent function as follows:

In this function, Orb_ht_cm is the height of the orbit of each subject standing in front of the platform or obstacle, and Step_x_cm is the step amplitude from starting position (standing in front of platform or obstacle) to end position (foot on platform or foot at the far side of the obstacle).

Finally, the Gaze Error Index was measured as the discrepancy between the participants' actual gaze angle and the gaze angle to footfall, as follows:

Gaze Error Index values on the order of 90° indicate a tendency to look toward the horizon, whereas values approaching 0° an actual gaze angle approximating the gaze angle needed to fixate the footfall location in the saggital plane. An improvement in our participants means a lower Gaze Error Index.

Procedures 

Tracking of foot and head motion was done with 6-degrees-of-freedom electromagnetic sensorsa fixed with electrode tape to the dorsum of each foot and also to the back of a headband apparatus at the level of the occiput. The headband apparatus held an infrared oculography system25,b and an eye tracking camera.c Eye movement recordings of the right eye were obtained with the infrared system, which was synchronized to the motion analysis system. Images of the left eye were obtained with the eye camera. The eye images were used to help identify blinks and eyelid artifacts in the eye record. The position of the eye tracking camera was lateral to the eye to avoid obstruction of vision.

Infrared oculography data was sampled at 600Hz, and kinematic data were collected at 100Hz and then resampled up using a polyphase implementation interpolation technique based on Matlab technical programming code (version 6.5).d Head and eye data were filtered offline using a 10-Hz low-pass, 0 phase shift 2nd order Butterworth filter.

Blink artifacts in the oculomotor recordings were replaced by interpolating values constructed from the data before and after the occurrence of the artifact. The interpolation was based on a cubic spline.26 Trials with a noisy baseline or trace were eliminated. We also eliminated trials with eye velocity over 200° a second, because most of those trials showed signal artifacts that artificially inflated the eye velocity measurements. In addition, trials with eye velocities in that range were 3 SDs beyond the average for this cohort, and therefore they were considered abnormal and eliminated. A total of 12 trials were excluded from the analysis.

Intervention 

The intervention was performed by a trained group of researchers supervised by the investigators of this study. A group of 10 physical therapy students administered the intervention. All treatment sessions were done in the motion analysis laboratory, Physical Therapy Department, at the University of Minnesota. The location of the intervention was minimized from sound and visual distractions. Participants in both groups received treatment 3 times a week for 1 hour for 4 weeks. The duration of intervention was decided based on the literature reporting rehabilitation for PD27 and also on standard practice adopted by local rehabilitation clinics. Each group received a common and a group specific set of exercises.

Common exercises 

The common set of exercises performed by both groups included tandem stance practice with eyes open and closed, turning 360° while marching in place, and sit-to-stand and stand-to-sit practice on a chair. These exercises were based on a falls prevention program for older women developed by Findorff et al.28 In addition, participants practiced corrective postural reactions to gentle perturbations backwards. Trainers pulled the participants' shoulders or hips with enough strength to evoke protective steps backward. A similar technique has been used to improve postural instability and gait in patients with PD.27, 29 The common exercises were performed by both groups once a week for 1 hour. See Zampieri and Di Fabio19 for details. Each group also received a supplemental set of exercises 2 times a week for 1 hour.

Group-specific exercises 

Participants in the treatment group received eye movement plus visual awareness training as a supplemental activity. In order to develop this protocol, we modified protocols from different studies on rehabilitation of patients with oculomotor deficits but without PSP. In order to improve visual awareness of our participants, we developed a scanning exercise based on techniques used for patients with visual neglect caused by stroke.30, 31 This practice consisted of scanning the environment to identify hidden objects. In order to improve saccadic eye movements, we used computer-assisted saccade exercises in which participants had to respond with a key press to visual stimuli presented in random locations on the computer screen. For this practice, we used software developed by the Optometric Extension Program Foundation,e which has been mainly used to improve reading skills in the general population. Auditory feedback was also used to encourage participants to increase ocular range of motion by producing different sounds.32 This technique has been proven successful in the rehabilitation of congenital nystagmus.33 Finally, our protocol also involved a stimulus-response compatibility paradigm with the objective of improving attention and enhancing eye-foot coordination. This paradigm has been developed and tested in our laboratory11 with elderly participants. The supplemental exercises were performed 2 times a week for 1 hour. For details, see Zampieri and Di Fabio.19 Supplemental activity for the comparison group consisted of additional supervised balance exercises for 2 sessions a week (1hr each). These exercises were also part of the falls prevention program by Findorff et al.28 These activities were performed 2 times a week for 1 hour. For details, please see Zampieri and Di Fabio.19

Statistical Analysis 

NCSS statistical softwaref was used to carry out our analysis. Data were tested for skewness, kurtosis, and omnibus normality. In all cases, hypotheses were nondirectional (Ho [null hypothesis]: no difference between means), and the critical α level was established at 0.05. A chi-square test was used to check for categorical baseline differences between groups. A 2-sample t test was used to compare continuous baseline measurements: disease duration, UPDRS-motor section,21 PSP Rating Scale,22 the gait section of the PSP Rating Scale, and Folstein Mini-Mental State20 baseline values.

To investigate changes after treatment, a 2-way repeated-measures ANOVA with group (treatment × comparison) as a between-group factor and test (pretest × posttest) as a within-group factor was performed on each dependent variable: vertical Gaze Fixation Score and Gaze Error Index.

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Results 

Baseline Measurements 

The baseline characteristics of our groups are shown in table 1. Measurements of disease severity by motor section of the UPDRS and the PSP Rating Scale indicate moderate stages of the disease. There were no significant differences between groups in terms of diagnosis (possible vs probable), sex, age, time of symptom onset, disease severity, and gait scores (a component of the PSP Rating Scale). A significantly lower Mini-Mental State score was observed for the treatment group. However, such difference was not considered important because the Mini-Mental State Examination was used as a screening tool to make sure participants would be able to follow instructions, and both groups reached the cutpoint of 23.

Table 1. Group Characteristics
VariablesTreatment GroupComparison GroupP
Diagnosis (possible/probable)2/84/5.25
Sex (men/women)5/55/4.80
Age (y)71.20±5.28(64–−83)67.55±7.28(57–78).22
Symptom onset (mo since first symptom was noticed)40.60±31.80(10–120)53.00±34.66(3–96).42
Folstein Mini-Mental State Examination25.70±1.05(24–28)27.44±2.04(24–30).02⁎
UPDRSm†19.90±6.74(11–30)22.11±7.33(10–34).50
PSP rating scale30.10±10.34(12–45)28.44±8.38(13–40).70
PSPg‡7.70±4.47(2–15)9.55±3.84(3–14).34

Note. Values are means ± SDs for continuous variables. Range of values is in parentheses. A t test was used to compare continuous variables, and a chi-square test was used to compare categorical variables.

⁎Significant difference between groups.

†Motor component of the UPDRS (maximum score, 56).

‡Gait subscore the PSP rating scale (maximum score, 20).

Between-Group Comparisons 

Figure 2 shows the vertical Gaze Fixation Score for both groups at pretest and posttest. Average values are shown in figure 2A, and individual values are shown in figure 2B. Our 2-way repeated-measures ANOVA showed a significant main effect of test (F1,17=6.98; P=.01) and a significant interaction (F1,17=2.57; P=.001), with the treatment group having a significantly lower vertical Gaze Fixation Score at posttest, and the comparison group having no significant changes between pretest and posttest. The decrease in vertical Gaze Fixation Score for the treatment group indicates an improvement in gaze shift ability. Because vertical Gaze Fixation Score pretest values for the treatment group were higher than the comparison group, an analysis of covariance was also run to explore the potential significance of pretest as a covariate. The results showed that the vertical Gaze Fixation Score was not a significant covariate influencing posttest vertical Gaze Fixation Score (F1,12.76; P=.10).

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  • Figure 2. 

    Vertical gaze fixation score. (A) Average pretest and posttest values for the treatment and comparison groups on vertical Gaze Fixation Score during the step-up activity. Values displayed as means ± SEs. (B) Individual pretest and posttest values. Each dot represents 1 subject (average of 4 trials). Arrow down indicates direction of improvement. *Significant difference with α<.05.

Figure 3 shows the Gaze Error Index for both groups at pretest and posttest. Average values are shown in figure 3A, and individual values are shown in figure 3B. There was also a significant decrease of the Gaze Error Index at posttest for the treatment group, indicating an improvement in ocular mobility, with no significant changes for the comparison group. Our 2-way repeated-measures ANOVA showed a significant main effect of test (F1,17=9.76; P=.006) and a significant interaction (F1,17=9.56; P=.006).

  • View full-size image.
  • Figure 3. 

    Gaze error index. (A) Average pretest and posttest values for the treatment and comparison groups on Gaze Error Index during the step-up activity. Values displayed as means ± SEs. (B) Individual pretest and posttest values. Each dot represents 1 subject (average of 4 trials). Arrow down indicates direction of improvement. *Significant difference with α<.05.

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Discussion 

This study compared the effects of eye movement exercises associated with balance training versus balance training alone on gaze control in patients with PSP. Our results show that participants who received eye movement exercise coupled with balance training improved their ability to shift gaze downward, whereas no changes were observed for participants who received balance training only (see Figure 2, Figure 3).

The improvement in gaze control observed in our group of subjects was accompanied by improvements in gait and general mobility. A detailed description of our findings related to gait and mobility is reported in a companion article.19 In that study, we found a significant increase in walking speed and a decrease in stance time in the group that received eye exercises associated with balance training. General mobility as measured by the Timed Up and Go test did not change significantly, but it showed a moderate effect size in favor of intervention. Fall episodes were not reported because we found it to be a biased measure because of the constant guarding by caregivers preventing patients from falling in many instances. Our results support the idea that gaze control is important in the control of locomotion, and oculomotor function can be improved with training even in a progressive neurodegenerative disease.

The neural systems responsible for the control of VOR suppression are thought to be in the frontal and parietal cortex. Ventre and Faugier-Grimaud34 have shown that unilateral lesions of the parietal cortex (area 7) of monkeys induced deficits in the suppression of the VOR in the horizontal direction. In cats, lesions with injections of muscimol, a neurotransmitter inhibitory drug, into the vestibular responding areas around the FEF caused difficulty suppressing the VOR in the vertical and horizontal direction.35

Similar observations have been reported in humans. Patients with diffuse cortical damage such as hemidecortication or hemispherectomy could not suppress the VOR during rotation toward the lesioned side, but could successfully do so when rotated toward the side contralateral to the lesion.36, 37 The same behavior was observed in patients with more localized lesions after ischemic strokes in the parietal, frontoparietal, and temporoparietal cortices.38

The frontal and parietal cortices are responsible for controlling not only VOR suppression but also purposeful gaze shifts to targets in the environment. Electric stimulation of the FEF in monkeys has been observed to elicit head movements together with saccadic eye movements toward the contralateral side,39 and unilateral ablation of the FEF has been shown to cause a deviation of the head and eyes toward the lesioned side.39 In humans, the FEF has been related to the triggering of voluntary saccades with the purpose of intentionally exploring the visual environment.40 The parietal cortex (parietal eye field), on the other hand, has been related to the generation of reflexive saccades.41

In PSP, there is degeneration in the frontal cortex42; however, the degree of neuronal loss is considered mild compared with the degeneration in the brainstem.1, 3, 42 The mechanism responsible for the deficits in VOR suppression in PSP is not well understood, but it has been speculated that it is a result of a preponderant activity of omnipause neurons in the nucleus raphe interpositus of the pons over weakened burst neurons in the rostral interstitial nucleus of the median longitudinal fasciculus of the midbrain.43

Given that the cortical areas responsible for voluntary control of VOR suppression are only mildly affected in PSP, plasticity must be preserved to some extent in those areas. We speculate that the eye plus balance intervention elicited predominantly the activity of the frontal cortex (FEF), because this structure is responsible for intentional gaze shifts, and our experimental set-up required voluntary gaze shifts to the footfall area beyond the platform, rather than reflexive gaze shifts to an intermittent target.

The literature refers to vicariation as the neuroplasticity mechanism in which the brain reorganizes to compensate for the loss of a certain area by having another area taking over the function of the damaged area. Such a process has been well characterized within cortical areas in animal models of stroke44 and also in humans with stroke.45, 46 Studies in humans show that, after damage of the primary motor cortex, the premotor cortex has the capability of taking over the function of the primary motor cortex.45, 46

Although cortical plasticity has not been demonstrated in patients with PSP, there is evidence of plasticity occurring in PD. Sabatini et al47 observed corticomotor reorganization in the primary motor cortex, inferior parietal cortex, supplemental motor area, and anterior cingulated cortex of patients with PD after practice of sequential manual movements. Another study by Hanakawa et al48 used brain perfusion images by computed tomography to show that treadmill walking with lines serving as visual cues elicited more activation of the lateral premotor cortex in patients with PD than controls. PSP shares many characteristics with PD. This literature supports the idea that parallel motor circuits involving the cortex can be recruited in such disorders to overcome functional deficits originated subcortically.

Study Limitations 

The lack of published rehabilitation studies addressing PSP has created a need for systematic investigations of the efficacy of intervention. One of the limitations of this study was the small number of subjects, which reduces statistical power. Given that PSP is a rare disease,2, 49 and it is often misdiagnosed as PD,4, 50 it was difficult to enroll a larger number of subjects. Visual awareness training and balance exercises can be easily incorporated into rehabilitation practice, but the precise methodology that we used in this laboratory-based study for ocular motor training might differ from feasible clinical application. Thus, it is not known at this time whether the translation of our method from laboratory to clinic will be effective. It remains to be investigated whether there are any carryover effects of the therapy. In addition, for the sake of experimental control, our protocol had participants starting a task from a standing still position, when in real life these activities are more likely to be performed during locomotion. More research is necessary to investigate gaze control behavior during locomotion. Our study investigated the immediate effects of 1 month of rehabilitation to improve gaze control in PSP. It is not known if there are any carryover effects of the therapy.

Future Studies 

Other patient populations have ocular motor control dysfunction that disrupts activities of daily living. These populations include cerebellar ataxia and other parkinsonian syndromes such as corticobasal degeneration.4 Future studies are necessary to determine whether the methodology used in the current investigation can be generalized to patients with these disorders.

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Conclusions 

Our study provided preliminary evidence that balance and eye movement training might be an effective therapeutic approach to improve gaze control in patients with PSP who are still ambulatory. Possible mechanisms to explain our findings may relate to the plasticity of the frontal cortex in these patients. It is not known how our intervention method translates from laboratory to clinic. Further research is necessary to determine the carryover effects of this therapy and to determine its effects on other populations.

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Appendix 

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References 

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  • a Innovative Sports Training Inc, 3711 N Ravenswood, Suite 150, Chicago, IL 60613.
  • b Microguide Inc, 1635 Plum Ct, Downers Grove, IL 60515.
  • c Arrington Research Inc, 27237 N 71st Place, Scottsdale, AZ 85266.
  • d The Mathworks Inc, 3 Apple Hill Dr, Natick, MA 01760-2098.
  • e Vision Builder Software, Helga Blystadsvei 8, 2316 Hamar, Norway.
  • f NCSS Software, 329 North 1000 East, Kaysville, UT 84037.

 Supported by the National Institute of Disability and Rehabilitation Research (grant no. H133G030159).

 No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit on the authors or on any organization with which the authors are associated.

 Reprints are not available from the author

PII: S0003-9993(08)01603-1

doi:10.1016/j.apmr.2008.07.024

Archives of Physical Medicine and Rehabilitation
Volume 90, Issue 2 , Pages 263-270, February 2009

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