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ORIGINAL ARTICLE
Modality-Specific, Multitask Locomotor Deficits Persist Despite Good Recovery After a Traumatic Brain Injury Bradford J. McFadyen, PhD, Jean-François Cantin, PhD, Bonnie Swaine, PhD, Guylaine Duchesneau, MPs, Julien Doyon, PhD, Denyse Dumas, PT, Philippe Fait, MSc ABSTRACT. McFadyen BJ, Cantin J-F, Swaine B, Duchesneau G, Doyon J, Dumas D, Fait P. Modality-specific, multitask locomotor deficits persist despite good recovery after a traumatic brain injury. Arch Phys Med Rehabil 2009;90: 1596-1606. Objective: To study the effects of sensory modality of simultaneous tasks during walking with and without obstacles after moderate to severe traumatic brain injury (TBI). Design: Group comparison study. Setting: Gait analysis laboratory within a postacute rehabilitation facility. Participants: Volunteer sample (N⫽18). Persons with moderate to severe TBI (n⫽11) (9 men, 3 women; age, 37.56⫾ 13.79y) and a comparison group (n⫽7) of subjects without neurologic problems matched on average for body mass index and age (4 men, 3 women; age, 39.19⫾17.35y). Interventions: Not applicable. Main Outcome Measures: Magnitudes and variability for walking speeds, foot clearance margins (ratio of foot clearance distance to obstacle height), and response reaction times (both direct and as a relative cost because of obstacle avoidance). Results: The TBI group had well-recovered walking speeds and a general ability to avoid obstacles. However, these subjects did show lower trail limb toe clearances (P⫽.003) across all conditions. Response reaction times to the Stroop tasks were longer in general for the TBI group (P⫽.017), and this group showed significant increases in response reaction times for the visual modality within the more challenging obstacle avoidance task that was not observed for control subjects. A measure of multitask costs related to differences in response reaction times between obstructed and unobstructed trials also only showed increased attention costs for the visual over the auditory stimuli for the TBI group (P⫽.002). Conclusions: Mobility is a complex construct, and the present results provide preliminary findings that, even after good locomotor recovery, subjects with moderate to severe TBI show residual locomotor deficits in multitasking. Furthermore, our results suggest that sensory modality is important,
From the Center for Interdisciplinary Research in Rehabilitation and Social Integration and the Department of Rehabilitation, Faculty of Medicine, Laval University, Québec (McFadyen, Fait); Center for Interdisciplinary Research in Rehabilitation of Greater Montreal and Montréal Rehabilitation Institute, Montréal (Swaine); School of Rehabilitation (Swaine) and the Department of Psychology (Doyon), University of Montréal, Montréal; and Québec Rehabilitation Institute (Cantin, Dumas, Duchesneau), Québec, Québec, Canada. Supported by the Canadian Institutes of Health Research (grant no. 64408). 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. Correspondence to Bradford J. McFadyen, PhD, Center for Interdisciplinary Research in Rehabilitation and Social Integration, 525 Hamel, Québec, Québec, Canada, G1M 2S8, e-mail:
[email protected]. Reprints are not available from the author. 0003-9993/09/9009-00190$36.00/0 doi:10.1016/j.apmr.2009.03.010
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and greater multitask costs occur during sensory competition (ie, visual interference). Key Words: Attention; Gait; Locomotion; Rehabilitation. © 2009 by the American Congress of Rehabilitation Medicine EING MOBILE IS CRUCIAL for independent living and B quality of life and is a major focus of physical rehabilitation programs. Mobility, however, is a complex construct not only requiring physical integrity related to the coordination of muscles and movements about many joints but also cognitive integrity to attend to and process sensory information and to plan and navigate the surrounding environment. Brain injuries, in particular a TBI, result in many different sequelae involving both cognitive and motor abilities that can affect one’s ability to navigate the complex environments found in daily life. Locomotor capacity and mobility after a TBI have not been studied nearly as often as with other populations with neurologic impairments (eg, stroke, cerebral palsy). Yet, work is emerging across different injury severities showing changes in dynamic equilibrium after mild TBI1 annd slowing and cautious walking after moderate and severe TBIs.2,3 The study of combined cognitive and walking ability has been performed by using different dual-task paradigms.4,5 Using such paradigms, it has been well established that walking requires attention6 and that this attention level is dependent on physical factors such as gait speed7 and personal factors such as age.5 Dual-tasking deficits after certain impairments have also been studied although the majority of existing work has concentrated on cognitive impairments caused by dementias or motor impairments (eg, Parkinson’s disease).4 Despite sequelae in both cognitive and physical functions after TBI, the study of dual tasking in this population is only very recent. Studying persons with trauma-related concussion, Parker et al8 showed acute effects related to shorter stride lengths when attention was divided by using verbal fluency or mathematic tasks. The same general protocol was repeated over 4 periods, from 48 hours to 28 days, after a concussion1 showing deficits in dynamic equilibrium and dual-task effects persisting up to 1 month after the concussion. Finally, Catena et al9 confirmed that dual tasking, using a “question and answers” task during gait, distinguishes concussed subjects from control subjects. To our knowledge, only 1 other study has looked at more severe cases of TBI by using a dual-task paradigm. Vallée et al10 have shown that persons with good recovery from moderate to severe TBI had residual deficits in both walking and cognitive performance that was most evident when in more complex environments related to avoiding wider obstacles and
List of Abbreviations TBI
traumatic brain injury
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performing the Stroop word task. In a related publication from the same study, Cantin et al11 also provided the first evidence that neuropsychologic tests of visuospatial deficits after TBI correlate to obstacle clearance margins during adapted gait showing some predictive ability of neuropsychologic tests for executive dysfunction during locomotion. One other study,12 although not looking directly at dual or multitasking, also showed greater variability in spatiotemporal gait parameters in subjects with TBI with increased complexity of the locomotor task (ie, walking fast or with eyes closed). Many of the studies on dual tasking during walking have used a wide range of simultaneous tasks including verbal fluency, arithmetic calculations, other motor tasks such as carrying other objects, and reaction times to auditory and visual stimuli. The latter 2 tasks correspond to most daily environments in which the processing of many visual and auditory stimuli is required while mobile. Most environments, whether public (eg, on the street) or private (eg, in the home), offer many visual stimuli that can be either related (eg, signs for direction) or unrelated (eg, other people, objects, and so on) to one’s mobility. Locomotion itself relies heavily on vision for its control even in direct straight-ahead walking.13,14 When the physical environment is more complex, such as in the presence of obstacles, visual control is important for safe lower-limb trajectories.15 It is now known that visual sampling of obstacles is performed 2 to 3 steps from the obstruction16 and that lead limb clearance (first limb to cross an obstacle) involves visual control, whereas trail limb clearance (second limb to cross) is more reliant on feedforward information and kinesthetic control.15 Auditory information, such as engaging in a conversation with another person or listening to a public announcement, is also common during locomotion and has been shown to involve dual-task effects during walking. For example, Lajoie et al6 showed decreased reaction times to an auditory signal during walking as compared with standing or sitting. They even found that attention was phase dependent with greater reaction times when the auditory signal was presented in the swing phase. Gérin-Lajoie et al17 have shown that circumventing an obstacle is affected by a simultaneous auditory task such that young adults provide more clearance of the obstacle when listening to the auditory message. These dual-task effects were also shown to be accentuated with age.18 Anecdotal information from clinicians often refers to the levels of distractions caused by auditory stimuli while working with patients having suffered a TBI, but no study to date has looked specifically at modality issues. Overall, little is known about the differential effects of the sensory modality of simultaneous tasks during walking. Of the few studies that have looked at simultaneous motor and cognitive tasks involving visual or auditory modalities, most involve standing postures. Recently, Woollacott and Vander Velde19 have shown in healthy, young adults that dual-task effects attributed to the visual system may be caused by visual code processing rather than simple visual interference. Yet, it would appear that with impaired postural control that any division of attention (whether from a visual or an auditory modality) will result in compromised balance.20 No study to date has directly considered auditory versus visual dual tasking during obstacle avoidance. Understanding locomotor mobility in complex environments with different sensory stimuli is important to improve rehabilitation interventions aimed at recovering function and social participation for persons with a TBI. The purpose of the present work was to build on our previous research3,10 studying the ability of persons with TBI to avoid obstacles and to specifi-
cally address, for the first time, the different influences of simultaneous tasks involving visual or auditory sensory modalities. As in our previous articles,3,10 we have focused on persons who had recovered their locomotor skills and were relatively independent and mobile in order to highlight residual and persisting impairments salient to moderate and severe TBIs. It was expected that despite good recovery, when simultaneous visual or auditory tasks are presented during the execution rather than the planning phase for obstacle avoidance, that subjects with TBI would persist in showing cautious gait behavior (slower walking and higher obstacle clearances) and show greater multiple task effects for visual interference but still general attention deficits regardless of sensory modality. METHODS Participants A convenience sample of persons who had a TBI and were either receiving or had received treatment from the multidisciplinary team at the TBI unit of the Quebec Rehabilitation Institute was recruited. These subjects had suffered only 1 TBI and had severity ratings after their accident of moderate or severe based on a combination of the hospital admission Glasgow Coma Scale score, duration of posttraumatic amnesia, length of the loss of consciousness, and interpretation of the neuroradiologic examination.21 In addition, subjects had to be considered to be independent for walking and to walk at speeds greater than 1.0m/s without assistance or technical aids. Subjects with skull fractures or open head injuries, cognitive or behavioral problems affecting their participation, or any other neurologic or musculoskeletal problems affecting their locomotion were excluded from the study. A convenience sample of control subjects was also recruited from the Quebec Rehabilitation Institute and university communities. These subjects were required to have no self-reported physical or neurologic problems and were matched on average for age and sex to the TBI group. Finally, all subjects had to show normal or corrected-to-normal visual acuity as measured on a Snellen test, normal hearing as verified by an audiologist at the Quebec Rehabilitation Institute, and ability to understand and read French. The latter was confirmed by the tests in audiology as well as by their understanding of instructions and performance on cognitive tests before data collection. Subjects also indicated that they could differentiate the 3 colors used for the visual task (see below) before testing commenced. The study was approved by the ethics committee of the Quebec Rehabilitation Institute, and all subjects signed a consent form before participating. Instrumentation Subjects wore their own comfortable walking shoes and clothes (loose pants were allowed) for the study. Triads of noncollinear infrared markers were placed on each subject’s head, trunk, and each foot. Kinematic data were collected by using 3 Optotrak sensor bars (model 3020a) at a frequency of 100Hz. Toe points were statically digitized before collection to reconstruct their trajectories from foot markers later. Verbal responses to the cognitive task (described later) were recorded through a microphone worn by the subject. Voice signals were amplified by using a channel mixer (MDR 6b) and then captured on both a computer (1000Hz) and as part of a video recording for each trial. A separate computer provided the visual and auditory stimuli to the subject and to the dataacquisition computer simultaneously. The visual stimuli were presented to the subject simultaneously on five 43.2-cm (17in) Arch Phys Med Rehabil Vol 90, September 2009
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Fig 1. Experimental setup showing the walking path, obstacle placement, force plate used to trigger both cognitive tasks (arrow), and orientation of computer monitors presenting the visual Stroop task.
flat screen computer monitors (Compaq 1720c), 2 pairs forming the sides of the walking path (approximately 1.6-m wide and 11-m long in total) and 1 monitor at the end (fig 1). This arrangement allowed subjects to get visual information without moving their head too much from their desired focal point. A video splitter (ST128PRO 8d) allowed the maintenance of signal quality across the monitors. A 6th screen placed out of the sightline of the subject had a photo sensor attached to it and was used to acquire the exact timing of the visual signal presentation. The auditory signal was sent to both a set of wireless headphones worn by the subject and to the acquisition computer. The volume of the headphones was fixed at the same level (80db) for all subjects by using a calibration tone and a sound-level meter (model 33-2055e). Protocol All subjects were evaluated by using separate clinical tests of executive function and attention as well as of balance and gait ability in addition to the laboratory evaluation. The significant neuropsychologic results of the Delis-Kaplan Executive Function System Trail Making Tests and of the Test of Everyday Attention will be presented along with the laboratory results. In the laboratory, subjects were required to walk over the 11-m walkway at natural speeds with and without an obstacle placed in the middle of the walkway. The obstacle, when present, was 122-cm wide and set in height and depth (length) to 15% of the Arch Phys Med Rehabil Vol 90, September 2009
leg length of the subject and was placed approximately 5 to 6 steps from the starting position. The obstacle was made of a metal frame with a vinyl roller window shade that could be rolled out over the frame to form a box shape (see fig 1). We have used normalized obstacle heights in our studies3,10 to allow us to compare similar tasks across subjects. Fifteen percent of leg length is similar to a street curb and known to elicit anticipatory adjustments.3 Simultaneous visual or auditory stimuli were presented as described previously at a frequency corresponding to their average unobstructed stride time on half the trials. These stimuli were initiated at right heel contact in the middle area of the walkway by using a force plate and a force trigger threshold of 15N. This position corresponded to 2 steps before the obstacle when it was present. Therefore, during obstacle avoidance, the dual task was initiated at lead (first limb to clear the obstacle) foot contact before its clearance followed by trail limb clearance. The visual stimulus was adapted from the Stroop Word test commonly used in neuropsychology,22 presenting a single word on the monitors that indicated 1 of 3 colors in the same or different color as their lexical meaning. Subjects were asked to name the color of the ink of the word and to ignore the meaning of the word. This test was chosen because it provides a visual task not requiring memory. The auditory task was a modified version of the Stroop test in which the words “man” or “woman” were pronounced by either a man or woman through the earphones requiring subjects to name the speaker’s sex and not the word heard. Therefore, again, subjects had to ignore the lexical meaning. All subjects were allowed to practice the Stroop tasks ahead of time and to perform each walking condition (with and without obstacle, with and without dual task) before data collection began. All subjects began with the unobstructed walking conditions to ensure the attainment of comfortable walking speed. For the subsequent walking trials, obstacle and dual-task conditions were presented in blocks of 5 trials and counterbalanced across subjects. We informed subjects of the presence and modality (visual or auditory) of the stimulus before each trial and instructed them to respond as fast as possible when it was present. Data Analyses Kinematic data were filtered by using a second-order Butterworth, zero lag filter with a cutoff frequency of 6Hz. An average of each dependent variable was calculated across trials for each subject to be used for statistical analyses. Dependent variables analyzed included performance on the cognitive task related to response reaction times to the Stroop stimuli (calculated difference between first stimulus and response onsets) and multitask costs comparing response reaction times between obstructed and unobstructed walking (therefore, between dual and triple tasking, the latter involving an adjustment for the obstacle at the same time as performing the cognitive task) and performance on the locomotor task including walking speed (average speed of the body center of mass over lead and trail strides with and without obstacle) and foot clearance margin (distance of the foot above the obstacle normalized to obstacle height). In addition, intrasubject variability using the standard deviation values across trials for a subject was analyzed. Nonparametric statistical tests were used because they are more conservative than their parametric counterparts and because of the limited homogeneity of the data among the TBI group. Differences between groups were tested with the MannWhitney U test. For comparison across conditions within groups, a Friedman test was first applied to test for any general differences across conditions (except for the multitask costs in
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MULTITASK DEFICITS AFTER TBI, McFadyen Table 1: Characteristics of the TBI Subjects and Medians and Interquartile Ranges for Both Groups N
Sex
Age (y)
BMI
GCS* (/15)
PTA† (d)
Time‡ (mo)
Gait Speed (m/s)§
1 2 3 4 5 6 7 8 9 10 11 Median (IQR) CNTL Median (IQR)
M M M F M M F F M M M
17.03 38.09 17.41 56.44 26.8 30.34 42.91 33.27 52.87 47.13 50.83 38.09 (20.41)
20.7 19.5 22.1 21.8 19.4 25.72 31.02 18.94 19.38 29.07 24.5 21.78 (5.67)
5 3 3 10 4 6 4 3 6 13 6 5.0 (2.5)
37 21 25 7 20 13 77 16 7 15 4 16 13
6.02 2.66 2.83 4.27 1.45 3.19 124.83 2.1 2.1 1.22 24.16 2.83 (3.04)
1.58 1.49 1.17 1.58 1.55 1.64 1.40 1.47 1.52 1.41 1.64 1.52 (0.14)
40.21 (21.55)
24.11 (3.48)
NA
NA
NA
NA
Abbreviations: BMI, Body mass index; CNTL, Control; F, female; IQR, interquartile range; M, male; NA, not applicable. *Lowest Glasgow Coma Scale at accident site or hospital. † Number of days of posttraumatic amnesia. ‡ Number of months since injury. § Clinical measure of gait speed over 10m.
which only 2 comparisons were necessary). When significant condition effects were detected, a Wilcoxon test was used for further pair-wise comparisons. We set significance levels to 0.05. Although a number of comparisons were made in this exploratory study, any corrections used to minimize type I errors would have also increased the risk of type II errors. Accepting both arguments and maintaining our previous practice,3,10 all alpha values of significant comparisons (ie, Pⱕ.05) were disclosed for the reader. RESULTS Final recruitment resulted in 11 persons with TBI and 7 control subjects for group comparisons. All subjects were white and French speaking. Table 1 shows the characteristics of the TBI subjects along with the group medians for the control group. There were no differences between the TBI and control groups for average age or body mass index (both with P⬎.05). The control group with 3 women did have a different female:male ratio (3:4 vs 2:9), but this was the only difference, and, to our knowledge, sex differences have not yet been shown for obstacle avoidance to date. The subjects with TBI were found to have executive dysfunction and visuospatial attention deficits as compared with control subjects. Specifically, the TBI group had significantly higher scores on visuospatial Trail Making Tests 1, 3, 4, and 5 and on the telephone search component (item 6) of the Test of Everyday Attention (P⬍.05) (table 2). The laboratory protocol was designed to provide each stimulus at a frequency equal to approximately the average stride time during unobstructed walking. Therefore, the stimuli should be triggered around each right heel contact. It was found post hoc that this was the case. The first stimulus (stimuli 1) was presented just after heel contact (approximately at 35ms for the visual stimuli and 54ms for the auditory stimuli). The second stimulus (stimuli 2) presentation was always around second right heel contact although slightly more variable across conditions and trials because of the inherent variability in gait speeds. The response onsets for stimulus 1 were always in the early part of the left stance phase around right toe-off (ie, at the beginning of lead obstacle clearance). Response onsets for stimulus 2 were, like
this stimulus’ presentation, a bit more variable being either at the end of left swing after trail obstacle clearance or in early left stance with no obstacle present. There were no differences in gait speed between groups for any condition (fig 2A, B), and, if anything, the subjects with TBI tended to walk faster. Only the TBI group showed general differences across conditions (2⫽29.338, P⬍.001). Further analyses showed that these subjects slowed their gait speed slightly from the single walking task to the visual (P⫽.012) and auditory (P⫽.001) dual tasks for unobstructed walking (see fig 2A) and slowed from unobstructed walking to obstacle avoidance for each respective condition (no simultaneous task, P⬍.001; visual task, P⫽.012; auditory task, P⫽.007). For intrasubject variability in gait speed (fig 2C, D), there was only 1 group difference during unobstructed walking with the simultaneous visual task (P⫽0.044) because of a decrease by control subjects for this condition from the unobstructed walking (see fig 2C). There was also a general difference across conditions for the TBI group (2⫽20.974, P⫽.001) but not for the control group. Specifically, variability in speed for the TBI group was significantly decreased for obstacle avoidance for the conditions without stimulus (P⫽.021) and with visual (P⫽.003) and auditory stimuli (P⫽.027). Subjects with TBI also showed a significant decrease between the no simultaneous task and the simultaneous visual task but only during obstructed walking (P⫽.042). Table 2: Medians, Interquartile Ranges, and P Values Between Neuropsychologic Test Scores of the TBI and Control Groups Tests
TBI Scores
Control Scores
P Value
TEA 6 TMT 1 TMT 3 TMT 4 TMT 5
3.9 (1.31) 21 (6.5) 34 (16.5) 76 (24.5) 26 (5.5)
2.6 (0.37) 12 (3.0) 23 (4.0) 54 (20.5) 20 (5.0)
.01 .04 .04 .04 .04
NOTE. Interquartile ranges are in parentheses. Abbreviations: TEA, Test of everyday attention; TMT, D-Kefs trail making test.
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Fig 2. Walking speeds (A, B) and intrasubject variability in walking speeds (C, D) during unobstructed and obstructed walking. Data are indicated for subjects with TBI (dark boxes) and control subjects (pale boxes) with no division of attention and with simultaneous visual and auditory Stroop tasks. The box plots indicate medians (thick horizontal bars), the 75th (top of box) percentile range, and 25th (bottom of box) percentile range, whereas I-bars indicate full ranges. Outliers (empty circles) represent values that were at least 1.5 times greater or less than the interquartile range. Significant differences (P
