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Journal of Neurologic Physical Therapy:
doi: 10.1097/NPT.0b013e31814a6493
Article

Attention and Dual-Task Conditions: Physical Therapy Implications for Individuals With Acquired Brain Injury

McCulloch, Karen PT, PhD, NCS

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Author Information

Division of Physical Therapy, Department of Allied Health Sciences, School of Medicine, University of North Carolina, Chapel Hill, Chapel Hill, North Carolina

Address correspondence to: Karen McCulloch, E-mail: karen_mcculloch@med.unc.edu

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Abstract

The aim of this article is to consider how impairments in attention may affect the performance of two tasks during balance or walking in individuals recovering from acquired brain injury (ABI). Guidelines from the experimental dual-task paradigm from cognitive psychology are reviewed. In this paper, dual-task conditions are described as the use of two tasks performed simultaneously, but not necessarily following all the experimental guidelines of the dual-task paradigm. How and why dual-task costs may emerge are discussed as well as considerations for task selection. Review of literature that describes dual-task performance problems in older adults is summarized briefly as a foundation for considering how similar conditions may affect individuals with ABI. Studies of individuals with ABI of dual-task performance in balance or walking are reviewed in detail. Examination approaches including observational measures of attention as well as clinical measures of dual-task performance during walking are reviewed. Intervention concepts and approaches are described by review of intervention designs used with older adults and individuals with ABI that describe task selection and use of instructional set for dual-task training. Two intervention strategies described in the literature for treating attention problems are contrasted: (1) an explicit focus on cognitive impairments with the expectation that function will improve as a result and (2) an implicit focus on functional tasks through errorless learning with the expectation that cognition (and attention) will improve. An illustration of the use of both of these strategies in a complementary fashion to improve attention in a patient with ABI is reviewed. Current literature is limited in clearly directing assessment and intervention to improve attention after ABI, but strategies are presented and areas for future research are identified.

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INTRODUCTION

Impairments in postural control and mobility are often an important focus of neurologic physical therapy (PT) intervention. In recent years, the interplay between attention and postural control or walking has been a growing topic of research with older adults.1 Much of this research requires individuals to balance in standing or to walk while simultaneously performing another task (cognitive or motor). These dual-task conditions illustrate how older adults divide attention between two tasks. Difficulties with dual-task performance are associated with a history of falls2–4 and risk of future falls in institutionalized5,6 and community-dwelling7 older adults. Patients with neurologic involvement often have cognitive deficits, balance deficits, or both, and the risk of falls is a common concern. An understanding of how attention and mobility interact to affect balance and safety in patients with neurologic impairment is an important goal.

Attention is a multifaceted cognitive construct that is manifest in many ways. Hart et al8 described components of attention including “arousal, alertness and orienting, focused attention and internal/external distractibility, cognitive speed, sustained attention, vigilance and persistence; working memory and attention span; shifting and dividing attention; initiation, performance consistency and ability to mobilize and direct attentional resources” based on observations of individuals with traumatic brain injury (TBI). Research to understand how this extensive range of cognitive abilities affects balance and walking is growing and has focused primarily on divided attention using dual-task conditions.

The purpose of this article is to review literature illustrating how impairments in attention affect individuals with acquired brain injury (ABI), as well as to describe methods for examining divided attention in a PT context and discuss implications for intervention for patients with attentional impairments. The major sections of the paper include a review of the experimental dual-task paradigm and more general dual-task conditions (requiring divided attention). Literature that describes dual-task difficulty during standing balance or walking in older adults forms an important foundation for understanding ways to examine divided attention and are reviewed briefly. Evidence of attention problems after ABI are also summarized. Methods commonly used by therapists to describe attention as well as clinical tests of dual-task performance during walking or other motor tasks are reviewed. Intervention strategies that address attentional impairments are highlighted. Evidence to clearly direct PT practice remains limited, but examples from this growing body of literature provide insight into strategies for intervention.

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DUAL-TASK PARADIGM AND DUAL-TASK CONDITIONS

The methodology for experimental testing using a dual-task paradigm with motor skills is described in a classic paper by Abernethy.9 The dual-task paradigm (or methodology) provides information on “the automaticity, hemispheric locus and structural independence of processes hypothesized to underlie the production of skilled performance.”9 This experimental approach from cognitive psychology examines two tasks performed simultaneously (dual task). One of the two tasks is designated the primary task. Primary task performance is maintained at the baseline (single-task) level during the dual-task condition. If, in the dual-task condition, performance on the secondary task is reduced from the baseline level, it reflects high attentional demands of the primary task and suggests insufficient reserve capacity to perform the secondary task at the baseline level. Experiments using the dual-task paradigm typically use very sensitive measures of performance such as reaction time to detect small differences in performance from the single-task to dual-task situation. Although this experimental paradigm is useful to test attentional theory, maintenance of primary task performance at baseline levels is difficult to ensure, and laboratory experimental methods are not possible in clinical settings.

Studies assessing attention during balance or walking do not always adhere to experimental guidelines for the dual-task paradigm. A walking task may be combined with simultaneous performance of a cognitive or motor task. Either or both tasks may vary from the single-task performance level. This approach is described in this paper as the use of dual-task conditions. Two tasks are performed simultaneously, but without efforts to designate primary and secondary tasks, so maintenance of the primary task at baseline level is not a consideration. In addition, measurement and analysis of single-task performance of both tasks may not be a priority. Dual-task conditions are highly relevant in clinical practice. In the natural environment, patients often combine tasks necessary for daily life and may need to prioritize one task over another based on changing task or environmental demands (ie, recall the correct phone number while walking or pay more attention to walking over an uneven surface to prevent a fall).

An example of dual-task performance in the PT context will illustrate how methods from the experimental dual-task paradigm can be applied to dual-task conditions to improve objective measurement of patient performance. Let us consider a 10-m walking task combined with a serial subtraction task (subtract threes from a number between 100 and 200). Consistent with dual-task methodology, single-task testing of walking (recording time) and subtraction (recording the percentage of accurate responses) would occur first, so (1) the ability to complete each task singly is ensured and (2) the effect of the dual-task condition may be evaluated.9 The ability to walk and subtract threes at the same time, or dual-task performance, is observed with measurement of walking time and cognitive task accuracy using the same methods as in the single task condition. In the dual-task condition, there is a range of possible responses. Walking could be slower, more variable, or less stable; subtraction could be slower, less accurate, or not completed at all. Reductions in performance could occur in neither, one, or both tasks.

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Dual-Task Costs

Reduced performance in the dual-task condition is described as dual-task cost (DTC) (or deficit). DTC may be expressed as a difference between the single- and dual-task performance or absolute DTC. Absolute DTC can be influenced by the rate of baseline performance. For instance, walking DTC for a patient who walks very slowly may be much greater than for someone who walks quickly. To account for baseline differences in single-task performance, an alternative metric is used, described as relative DTC.9 The relative DTC for walking time can be computed with this formula:

Equation 1
Equation 1
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This calculation controls for baseline performance, and dual-task performance costs are interpreted as a percentage (eg, 15% slower walking speed and a 25% reduction in cognitive task accuracy). This type of calculation allows for comparison across individuals or groups and also allows for comparison over time when baseline performance may change. Since the relative DTC can be computed for each task, the priority of performance of the motor or cognitive task is also apparent. The task with smaller DTCs appears to have been a priority. In order to analyze task performance at this level, measurement of motor and cognitive tasks in single- and dual-task conditions is necessary.9

DTCs are theorized to occur for several possible reasons: (1) structural interference (common resources are needed for each task, so resources allocated to one task cause poorer performance on the other)9; (2) limited capacity to attend to both tasks (insufficient attentional capacity to divide attention between balance and a cognitive task or capacity limited by information processing speed)10; or (3) difficulty with allocation of attention to both tasks. Of course, problems with any combination of these factors would also result in increased DTC.

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Allocation of Attention

Baddeley's model of working memory11,12 provides a framework for understanding allocation of attention that is necessary for divided attention tasks. This model includes three major components: the central executor and two slave systems, the phonologic loop (for auditory information) and visuospatial sketch pad (for visual and visuospatial information). The central executor allocates attention to incoming visual or auditory stimuli so that information can be processed and acted on or saved for later use. After coining the term working memory, Baddeley has since reflected that working attention may have been a better descriptor for the model.13 How this model applies to attention allocation for simultaneous cognitive and motor tasks is not completely clear.

The allocation of attention is perceived as an executive function task and is thought to involve the dorsolateral prefrontal cortex to direct attention to specific tasks. Imaging studies during executive control tasks also demonstrate increased activity in the basal ganglia–prefrontal–basal ganglia loop, superior parietal cortex, anterior cingulate, thalamus, and cerebellum during allocation of attention. Specific structures involved in executive control vary based on the cognitive task(s) chosen.14–17 Patients with prefrontal cortex pathology and impaired executive function skills may have difficulty with dual-task performance, when attention must be allocated to manage tasks simultaneously. Patients with motor involvement may also exhibit dual-task performance difficulty if balance or walking tasks require attention.

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Task Considerations for Dual-Task Conditions

Therapists can influence the priority of one task over the other during by using instructional set, directing patients to prioritize attention on one task (eg, “While you are walking, I want you to concentrate on not making any subtraction errors.”) or to attend to both tasks equally (eg, “Pay equal attention to walking and subtraction as you do them together. Do your best on both tasks.”). The degree to which these instructions are followed to prioritize one task over another may vary. Whether patients with ABI can follow such instructional set directives when cognitive and mobility tasks are combined is also not clear.

Patients may derive their own priority for attention to tasks when asked to do two things at once. Shumway-Cook et al2 described the “posture first” concept with older adults, suggesting that posture may take priority in dual-task conditions when a balance or mobility task is combined with a cognitive task. This priority on balance and posture is related to safety, but may be influenced by task demands, instructions, or patient goals. Such a priority in attention for balance may or may not be true for patients with neurologic involvement.18

Task characteristics are very important in dual-task conditions.19 The familiarity or novelty of a task and task difficulty play critical roles in how two tasks are performed at the same time. Overlearned tasks may be easier to combine with other tasks. Very simple tasks may be easily accomplished and well within available attentional capacity so that no DTCs are observed. Difficult or novel tasks may require additional attention to accomplish. Cognitive tasks that require language or mathematic skills may be more challenging for individuals with lower education levels. Tasks that require verbal responses may be disproportionately difficult for patients with aphasia or dysarthria. In order to interpret complex responses to dual-task conditions, therapists must pay careful attention to task type and difficulty.

Modes of stimulus input (auditory, visual, or kinesthetic) and response (verbal, motor) are also critical in choosing tasks for combination. If similar modes are necessary for input or response, structural interference may occur.9 For instance, if both tasks require visual processing, such as a visual discrimination task and a challenging postural control task that benefits from visual fixation, structural interference occurs in the visual system and performance of one task (or both) may suffer. If two tasks require motor responses, brain structures necessary to program and execute those responses may overlap and interference may occur.

The concepts of controlled processing and automaticity19,20 are important for patients with neurologic involvement. Controlled information processing is slow, deliberate, and effortful. Automaticity occurs when sufficient skill is attained that a task requires little attention, so a secondary task can be performed at the same time with ease. Tasks that may have been automatic prior to a stroke or brain injury, such as standing balance or walking, become more attention demanding and are no longer automatic after ABI. To improve unskilled control, cognitive processing must be employed, but with sufficient practice, tasks can become skillful and more automatic,20 although patients may never return to preinjury automaticity with some motor skills. This progression toward automaticity parallels stages of motor learning from cognitive, to associative, and finally autonomous stages21 and bears consideration when using dual-task conditions.

As skill improves, attention can be flexibly allocated to cognitive and motor tasks as is required. The use of dual-task conditions may encourage patients to use balance and mobility skills on a more automatic level or may simulate real-life situations (walking while finding one's way to a location in the rehabilitation center). There are times, however, when we must shift attention to focus on a particular task to a greater degree (eg, balancing while walking on an icy sidewalk or slippery floor) in order to be safe. This ability to flexibly allocate attention to the appropriate task enables function in a wider variety of scenarios including multitask situations. The presence of a problem with divided attention may therefore involve cognitive processes, a lack of motor automaticity, or problems in cognitive and motor abilities.

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DIVIDED ATTENTION IN STANDING AND WALKING

Dual-Task Performance in Older Adults

Current understanding of divided attention during standing and walking has been advanced significantly through the study of dual-task conditions with older adults. Findings from these studies are summarized briefly as a foundation to consider how patients with ABI may be affected in similar conditions.

Response time to secondary tasks increases as older adults perform more challenging postural tasks.22,23 The type and difficulty of the secondary task chosen are important factors. Several authors have described visuospatial tasks interfering with standing balance to a greater degree than other cognitive tasks.24–26 Tasks that require verbal responses also appear to degrade postural stability measured by center of pressure excursion. Sensitive force platform measures detect small changes in center of pressure associated with trunk muscle activation that occurs with phonation.27,28 Surface and visual surround manipulations, including sway-referencing, conditions employed in Sensory Organization Testing, also degrade standing stability in dual-task conditions.29–31 A secondary cognitive task reduces the recovery of postural stability,32–35 the ability to step over obstacles,36,37 and the ability to walk a narrow path.38,39 Attentional demands of walking may also influence safety for community mobility.40

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Improvement of Postural Stability in Dual-Task Conditions

Although reductions in standing postural control have been demonstrated in dual-task conditions in many instances, some studies have showed enhanced postural stability when secondary cognitive tasks are performed.41–43 The use of secondary tasks that require visual fixation may improve balance ability.44,45 Another explanation for improved postural stability during a secondary task relates to task difficulty and the constrained action hypothesis.46,47 This hypothesis suggests that a conscious focus on movement control constrains the motor system and interferes with automatic motor control processes that typically regulate movement. Use of an external focus of control, such as a cue to direct attention to the effects of movement, may allow the motor system to self-organize so that conscious control does not interfere.48,49

Low cognitive demand tasks have been associated with less postural sway in the dual-task condition when compared to the single-task “standing only” condition.50,51 Simple cognitive tasks paired with a standing task could benefit stability by facilitating a shift of conscious attention from balance, allowing more automatic execution. Huxhold et al50 theorized that the single-task standing condition may induce an internal focus of control as patients try to maintain stability. This conscious attention on standing balance may interfere with what should be an automatic process. However, as secondary task difficulty increases and resources necessary to accomplish both tasks may be in competition, a reduction in performance of either task may result. This contrast between internal and external focus of control may be important as therapists choose cues for patients during therapy after ABI.

Dual-task performance is not a simple issue to describe even with sensitive laboratory measures and careful use of the dual-task paradigm. The ability to document and analyze changes in the dual-task condition with clinical measures (without the benefit of laboratory equipment) in patients with neurologic impairment is challenging. If divided attention problems are severe, the effects may be easily observed (eg, inability to stand and talk at the same time). If problems in dual-task performance are more subtle, we may need to carefully apply methods from the dual-task paradigm to detect deficits.

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Dual-Task Performance in Patients With Neurologic Impairment

Many patient populations that neurorehabilitation therapists serve have difficulty with dual-task performance in cognitive/motor (upper extremity) and cognitive/cognitive task combinations as demonstrated by psychological research. Problems with dual-task performance have been described in patients recovering from TBI50–61 and mild brain injury or concussion.62,63 Following stroke, deficits in sustained, divided, and switching attention have been described.64–66 Patients who sustain stroke involving the anterior communicating artery may be particularly at risk of attentional problems59,67 because of possible damage to prefrontal cortex structures.

Patients with progressive diseases such as Parkinson's disease,14,68,69 Alzheimer's disease,70 and multiple sclerosis71–73 also have difficulty with dual-task performance. The cause of dual-task difficulties cannot be presumed to be the same across these diverse neurologic disorders, given different pathologies and behavioral characteristics. It is unclear how difficulties observed in cognitive psychology experiments relate to balance and walking in functional situations.

Dual-task conditions are pervasive in rehabilitation, extending to routine elements of therapy that require patient cognition. Dawes et al74 studied the effects of the concurrent cognitive task of rating intensity during a graded exercise test. Ten subjects with ABI and 10 healthy age-matched controls underwent a three-stage 50-rpm cycling exercise test. When subjects were asked to rate perceived exertion and shortness of breath, those with ABI slowed cycling cadence slightly, but not significantly. However, a difference in cadence between groups was observed in the most challenging stage of the exercise test, when the subjects with ABI slowed significantly. The authors cautioned that secondary cognitive tasks, even those routinely used in therapy, may cause decrements in performance, especially if exercise activity is less automated and at higher intensities. Physical therapists often use concurrent instruction during therapy activities including provision of feedback, sometimes asking patients to reflect and evaluate their own performance. The effect of having patients monitor their own performance may warrant further consideration.

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Dual-Task Balance and Walking

In a growing body of literature, researchers are investigating difficulties with dual-task performance in patients with neurologic involvement during balance or walking. The dual-task condition elicits decrements in cognitive performance,75 reduced postural stability,75–77 slowed walking,78 and increased walking variability79,80 across a range of patient types and task combinations. Considerable work has been undertaken to describe dual-task performance deficits with Parkinson's disease.81–87 Findings from these studies are not always consistent with results from study of dual-task performance in older adults. See Bloem et al18 for a recent review of how patients with Parkinson's disease may adopt a “posture second” strategy as opposed to the “posture first” concept described for older adults. This difference suggests that we must carefully study different types of patients, rather than assume older adult research will directly translate to patients with neurologic disorders.

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Acquired Brain Injury

Studies examining individuals following ABI,76,88–90 stroke,91–93 and TBI94–98 increase our understanding of how attention affects mobility during dual-task conditions. Haggard et al88 studied 50 individuals post-stroke or brain injury walking in single- and dual-task conditions while performing four cognitive tasks: word generation (category), paired associations, a visuospatial decision task, and mental arithmetic. DTCs were computed based on single-task performance. Costs were observed for stride duration (7%) and average cognitive task performance (4%). DTCs were significantly correlated with activities of daily living (ADL) function measured by the Barthel Index (r = 0.45) but not to 10-m walking time (r = 0.18). There were no differences in cognitive task performance based on hemispheric involvement for eight subjects with left cerebrovascular accident (CVA) and 22 subjects with right CVA.

Longitudinal follow-up of dual-task performance in two studies (16 subjects with ABI88 and 10 subjects with stroke90) documented greater improvement in single-task performance of walking and cognitive task performance than dual-task performance after rehabilitation.88 More improvement (eg, lower) in DTCs were observed for walking than for the cognitive task in their testing protocol.90 These results underscore the importance of testing tasks in combination and measuring cognitive and motor tasks in single- and dual-task conditions.

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Stroke

Harley et al76 investigated the effects of cognitive-motor interference on sitting balance after stroke. Using measures of seated postural sway, the effects of two tasks that required phonation were compared to single-task sitting in 36 patients recovering from stroke and 21 age-matched controls. The simple cognitive task involved repetitive utterance (ba-ba-ba) and the more complex task required generation of words in a category. Patients with stroke were less stable than controls in single-task sitting and demonstrated increased sway variability with both verbal tasks. This variability was inversely correlated with Barthel Index scores. Control subjects showed little change in sway variability with the repetitive utterance task, but variability increased significantly with the word-generation task. These findings suggest that even very simple verbal tasks may affect seated postural stability after stroke. The comparison to age-matched controls aids interpretation of changes that should be expected in dual-task conditions as opposed to DTCs that are a result of stroke.

Hyndman and Ashburn91–93 conducted a series of studies to systematically describe attention and dual-task performance during mobility after stroke. A sample of 48 community dwellers with chronic stroke (26 with right hemispheric stroke, 21 with left hemispheric stroke, and one with a brainstem stroke) underwent balance (Berg Balance Scale), ADL (Nottingham Extended ADL score), and attention testing (Test of Everyday Attention, and star cancellation for visual inattention). Fall history was categorized by frequency. Attention deficits were common in this sample of patients with stroke. Forty-three percent demonstrated divided attention impairment, 35% had visual selective attention deficits, and 31% showed sustained attention problems. Sustained and divided attention deficits were significantly correlated with balance, function, and fall history. Repeat fallers and nonfallers had significantly different scores for divided attention, balance, and ADL.91

The effects of a silent cognitive task (remembering a seven-item shopping list) on balance stability in standing and walking speed were studied for 36 patients with chronic stroke (mean, 16 months post-onset) and 24 age-matched controls.93 Subjects with stroke exhibited significantly more anterior-posterior sway in standing, slower walking velocity, and reduced stride length than controls in the single-task condition. In the dual-task condition, reductions in postural sway and gait slowing occurred in both groups. Group differences were only observed for walking time (slower after stroke). Cognitive task performance was maintained during standing balance, but degraded during walking trials for subjects with stroke. Subgroup analysis of fallers (n = 10) and nonfallers (n = 26) in the stroke sample revealed significant differences in stride length (shorter) and velocity (slower) for fallers. The cognitive task interfered with walking mobility to a greater degree after stroke, with reductions in walking velocity to 0.5 m/s for nonfallers and 0.4 m/s for fallers. This rate of walking may be insufficient for community mobility when secondary cognitive tasks may need to be performed.

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Traumatic Brain Injury and Concussion

Independently ambulatory individuals (n = 9) recovering from moderate to severe TBI were compared to nine age- and sex-matched controls while walking and stepping over obstacles (narrow and wide) with and without concurrent Stroop task testing.94 Subjects with TBI were slower with single cognitive task testing. Although the subjects recovering from TBI ambulated at 1.4 m/s on average in the single-task condition, in more complex motor (avoiding narrow and wide obstacles) and in the most complex dual-task condition, they were significantly slower than controls. Even individuals with very functional walking speeds may demonstrate DTCs with complex environmental conditions.

Additional studies of individuals with mild brain injury or concussion have shown increased postural sway in dual-task conditions,95,96 but reduced dual-task performance is not a consistent finding.97,98 Concussion may inconsistently result in cognitive or balance deficits. Unless preinjury test data are available for comparison, detecting deficits may be difficult.

Dual-task performance decrement during motor tasks is clearly a problem for patients with ABI, but has been more systematically studied after stroke than brain injury. Studies that characterize lesion location and use cognitive testing to confirm attention or executive control problems and relate those problems to difficulty in dual-task conditions are necessary. Findings are best interpreted with comparison to age-matched controls and use of single task testing of both tasks. The relationship between dual-task performance problems and risk of falls has preliminary support for patients with stroke, but is not clearly established for patients with brain injury.

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EXAMINATION CONCEPTS AND APPROACHES

Individuals with ABI often demonstrate problems with attention.8,62,64–66 Observation of attention is a critical part of the PT examination and may occur through the use of several standardized measures. Specific clinical tests of dual-task performance during walking are also described.

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PT Examination of Attention Deficits

The Guide to Physical Therapist Practice99 incorporates “arousal, attention, and cognition” as a component of tests and measures for all the neurologic practice patterns. The Guide recommends adaptability tests, arousal and awareness scales, indexes, profiles, and questionnaires to obtain necessary information about patient responsiveness and cognitive ability. Arousal, attention, and cognition are linked to functional limitations in self-care, home management, and fulfillment of life roles in work (job/school/play) and in community/leisure pursuits.99 Throughout the neurologic practice patterns, cognitive ability is related to safety for mobility tasks in home and community settings.

Specific measures that address arousal, including scales that characterize disorders of consciousness100 and agitation,101,102 have been reviewed elsewhere and are beyond the scope of this article. Arousal is a prerequisite to attention. Once aroused, patients can orient to stimuli in the environment and begin to use incoming information to make decisions about appropriate actions. Assuming a basic level of arousal is present, additional strategies to assess attention are necessary.

McDowd (this issue) reviewed a taxonomy of attention commonly used in clinical practice to classify task type: (1) selective attention: a focus on one source of information or task while not attending to other environmental distractions; (2) divided attention: concurrent processing of more than one source of information or performance of more than one task at the same time; (3) attention switching: alternating attention between two sources of information or tasks that share processing resources; and (4) sustained attention: maintenance of attention over long periods of time or vigilance.

If interdisciplinary team evaluations are conducted, therapists may seek information about these types of attention from (neuro)psychology, speech-language pathology, or occupational therapy evaluations. A variety of standardized tests are advocated to assess attention. One example is the Test of Everyday Attention,103 recommended in the Guide to Physical Therapy Practice,99 uses functionally oriented tasks such as map search for specific symbols (selective attention), listening to elevator tones to estimate floor level or lottery results (sustained attention), and searching a telephone directory in single- and dual-task conditions (divided attention). This test is marketed for use only by psychologists, speech-language pathologists, and occupational therapists.104 Shared results of standardized testing by multiple disciplines are necessary to determine the types of attention that are problematic for patients and to guide intervention.

Therapists commonly monitor patient behavior and make inferences about cognitive ability based on observation. The Rancho Los Amigos Levels of Cognitive Functioning Scale (RLAS)105 describes a hierarchy of cognitive and behavioral responses that are observed as individuals recover from brain injury. This eight-level scale includes multiple descriptors of behavior associated with each level of recovery. Table 1 provides descriptors from each level associated with attention and strategies for families to manage these attention problems.106 Recommendations involve reducing environmental distractions and reducing task or attention demands. These strategies are largely compensatory, modifying the environment and task demands to match attention deficits, like the approach of treating patients with attention problems in a quiet room. While the Rancho Scales appropriately guide families to manage behavior, it is not clear that compensation will facilitate improvement in attention. To prepare patients to return to functional environments that are often anything but a quiet room, these guidelines provide no suggestion for improving attention through therapy (eg, when to introduce more complex environmental conditions).

Table 1
Table 1
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Whyte et al107 developed a standardized assessment of attention for rehabilitation therapists to characterize behavioral responses after brain injury. The Moss Attention Rating Scale (MARS) originally incorporated 46 behavioral items associated with attentional problems. Following Rasch analysis,8 the scale was streamlined to 22 items rated on a 5-point scale (from 1, definitely false, to 5, definitely true). Items encompass three major factors: restlessness or distractibility, initiation, and sustained/consistent attention as described in Table 2. The MARS continues to be refined, but has good reliability and validity for measuring the behavioral complexities of attention. The MARS should prove useful as an outcome measure for rehabilitation teams to monitor attention in functional contexts. MARS items could also be used to characterize patient responses during PT activities when task complexity is increased.

Table 2
Table 2
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Cock et al89 studied patient awareness of attention problems with individuals recovering from TBI who were relearning to walk. Using a self-report questionnaire, patients described difficulty with dual-task conditions common in daily life (eg, making a list while walking). Patient and staff ratings were compared to gain insight into patient awareness of problems with attention. Staff ratings of patient divided attention difficulties were higher than patient self-ratings. Correlations of dual-task decrement during a walking task to ratings of dual-task difficulty were significant for several questionnaire items. The authors suggest that two questions may be candidates for screening patient awareness of divided attention problems: (1) “Would you find it hard to concentrate on the radio news while getting dressed?” and (2) “Would you find it hard to follow a television program at the same time as writing a letter?”

Scales that describe behavior may be useful for identifying types of attention that may be a focus for intervention or global assessment, but are not designed as PT-specific outcome measures. Clinical measures of dual-task performance during walking provide a more direct examination of how attention deficits affect mobility.

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Clinical Measures of Dual-Task Performance During Walking

Laboratory studies have demonstrated that balance is a task that requires increasing attention as people age by use of very sensitive measures of postural control and equally sensitive measures of response time to cognitive tasks.22–42 The functional ramifications of small changes observed with experimental methods are not completely clear, nor are laboratory measures feasible in routine clinical practice. Clinical measures of dual-task performance using observation and readily available equipment have been developed for older adults and may be useful for patients with neurologic involvement.

The Lundin-Olsson et al5 landmark paper on “stops walking while talking (SWWT)” identified institutionalized older adults who were unable to continue walking while talking at a significantly increased risk of falling in the next 6 months. This finding stimulated development of a number of clinical tests of dual-task performance during walking. These tests have targeted older adults primarily and include variations on the Timed Up and Go (TUG) with cognitive and manual secondary tasks,3,6 the Walking While Talking Test (WWTT),7 and the Walking and Remembering Test (WART).108–110 Bloem et al,111,112 after observing the lack of a relationship between fall risk and SWWT in patients with Parkinson's disease,113 developed the Multiple Tasks Test. Characteristics of these tests are described in Table 3.

Table 3
Table 3
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Hyndman and Ashburn92 studied the predictive value of the SWWT to identify falls in 63 people with chronic stroke. Twenty-six subjects had a positive SWWT on initial testing. Over the next 6 months, 16 subjects fell. The SWWT demonstrated 70% specificity and 53% sensitivity for identifying risk of future falls. Although the SWWT is a simple test to administer, the authors questioned the value of the SWWT as single indicator of fall risk for patients with stroke.92

We have conducted some comparison testing of clinical dual-task measures for people with ABI based on measures that we anticipated would be feasible and sensitive for a range of mobility and cognitive deficits.114,115 SWWT, WWTT, and the WART were compared for feasibility and ability to detect dual-task performance deficits in a population of ambulatory community dwellers with ABI.

The subjects were 18 ambulatory adults (five women) who were residents of a supported living program (n = 14), community dwellers (n = 2), and patients in acute rehabilitation (n = 2) who had sustained ABI, but were able to walk unaided (with or without an assistive device) for 40 ft. Subjects ranged in age from 24 to 58 years; 15 subjects were community ambulators and three ambulated at the household level. The household ambulators used assistive devices (two used walkers and one used a straight cane).

During a single testing session, the SWWT, WWTT, and WART were administered by trained raters. The SWWT was observed at the beginning of the test session and rated positive (stopped walking while talking) or negative (continued walking while talking). WWTT and WART order was counterbalanced for the sample. WWTT testing was administered as described by Verghese et al.7 Simple (alphabet) and complex (alternate letters of the alphabet) cognitive tasks were performed while walking at a self-selected speed for 40 ft (with one 180-degree turn at the midpoint). Consistent with dual-task methodology, walking was timed and letter accuracy was recorded in single- and dual-task conditions. Relative DTCs were calculated for cognitive and walking tasks based on single-task performance of each to allow comparisons across tests.

The WART included single-task testing of speeded walking on a 12-in. narrow path, 20 ft in length modeled after a laboratory test developed by Lindenberger et al38 Forward digit span was chosen as the concurrent cognitive task because task difficulty could be adjusted to challenge a range of working memory abilities. The tasks were combined during walking while remembering digits. Walking time, step accuracy, and cognitive task accuracy were recorded in single- and dual-task conditions. Relative DTCs were calculated based on single-task performance of the cognitive and walking tasks.

Summary findings are provided in Table 4. Although the SWWT was successfully completed by all subjects, the test result was consistently negative, so no DTCs were demonstrated. The WWTT walking task was completed by all subjects. The majority (87%) of the subjects could perform the simple cognitive task (alphabet) in the single-task condition, but only 44% were able to accurately perform the complex cognitive task (alternate alphabet). DTCs were elicited only for the complex cognitive task, but several subjects refused to attempt the complex task in the dual-task condition because it was so difficult.

Table 4
Table 4
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The WART walking task was accomplished by most subjects (94%), excepting one subject who had severe visual impairment and could not see the narrow path. Two additional subjects who were hemiparetic had difficulty remaining on the narrow path because of gait deviations. The cognitive task (forward digit span) was accomplished by all subjects, even those with severe declarative memory problems (forward digit span range, 2–7, mean, 4.5). Increased DTCs were demonstrated for both the cognitive and walking tasks.

For this small sample of individuals with ABI who were independently ambulatory with residual cognitive impairment, cognitive task difficulty was critical for test feasibility and the likelihood of eliciting DTCs. Very rote or simple tasks (talking, reciting the alphabet) were not sufficiently challenging for individuals able to ambulate at the household or community level. Walking task difficulty was also an important consideration. Speeded walking with a turn may provide sufficient challenge for ambulation, but did require a narrowed base of support that is difficult for some patients.

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Balance and Mobility Tests That Incorporate Dual-Task Conditions

A number of clinical tests of walking or balance use dual-task (walking with other motor tasks) or complex conditions. The Dynamic Gait Index115 and a modified version of the test, the Functional Gait Assessment,117 include items that require performance of two tasks (walking with head turning or nodding and obstacle avoidance). Additional development along this line has been described by Coppin et al.118 Walking combined with talking, picking up a package, carrying a package, stepping over an obstacle, and wearing a weighted vest were tested in older adults. Subjects who demonstrated greater difficulty in performing Part B of the Trails Making Test, a measure that requires attentional switching, had significantly greater declines in gait speed during the more complex dual-task conditions (carrying a large package, avoiding obstacles). If problems with more complex walking items are observed during examination, clinicians may decide to do further testing to assess dual-task performance using one of the clinical tests described in Table 3.

Therapists need to match patient motor, visual, and cognitive abilities to clinical measures of dual-task performance, so that tasks are feasible for patients to perform in the single-task condition. If tasks of appropriate difficulty are used in the dual-task condition, the interpretation of dual-task performance is more meaningful. The use of consistent tasks and conditions in subsequent assessments allows patient progress to be monitored. Additional study of clinical tests developed for older adults is necessary with individuals with ABI. With reliable and valid outcome measures that use dual-task conditions, therapists will be able to accurately identify dual-task performance problems and possible fall risk, establish guidelines for intervention, and judge whether intervention is effective in improving dual-task performance.

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INTERVENTION CONCEPTS AND APPROACHES

Therapists use a range of theories and frameworks to design intervention. In this area where our understanding of best strategies is developing, several ways of conceptualizing treatment of attentional problems are reviewed with evidence from intervention studies. The “person-task-environment” concept presented by Shumway-Cook and Woollacott116 and Gentile's taxonomy119 for task-environment characteristics are common starting points for intervention design. Study of older adults and patients with neurologic impairment are reviewed to illustrate how balance and attentional impairment are targeted in therapy through the use of dual-task conditions.

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Person-Task-Environment Interactions

The abilities of the patient (person) are considered carefully through the assessment of impairments and understanding of necessary activities and goals for participation. Therapists commonly manipulate task and environment factors during therapy using Gentile's taxonomy119 to increase therapeutic challenge. This taxonomy guides change in task and environmental factors to progress complexity. Object manipulation, a component of the taxonomy, provides a shift to dual-task conditions as secondary manual tasks are added to body stability or mobility tasks. As an illustration of this taxonomy-guided treatment progression, Rose and Clark120 described their 8-week (twice weekly) intervention trial to improve balance with older adults using the ProBalance Master. A progression of task difficulty began with single-task balance goals in sitting and standing on a firm surface with all sensory systems available. In subsequent weeks, task complexity was advanced by increasing balance challenge and modifying surface and visual conditions. By the fourth week of the intervention, dual-task goals were introduced with concurrent counting or reaching tasks during balance tasks. Balance was significantly enhanced in the intervention group as compared to controls, but the study did not include attention or dual-task outcome measures, so possible treatment effects on dual-task performance are unclear. Nevertheless, the treatment progression described in this study illustrates systematic modification of factors, including dual-task conditions, to increase patient skill in balance.

A case series by Silsupadol et al121 provides the most direct illustration of dual-task condition balance training, in addition to investigating the effects of instructional set on intervention. Three older adults with a history of falls were randomly assigned to one of three treatment approaches: single-task balance training, dual-task training with a fixed priority instructional set (directed to attend to both tasks equally at all times) and dual-task training with a variable priority instructional set (directed to attend to the postural task 50% of the time and to the secondary task 50% of the time).

Postural tasks were advanced using Gentile's taxonomy with stance and gait activities that incorporated environmental changes (closed versus open environments) and object manipulation. An extensive set of secondary cognitive tasks included: auditory discrimination, visual discrimination (pictures, Stroop); generation of items in categories, random digits, or complete sentences; subtraction (of numbers, letters); visual imagery tasks (describe directions, place letters/numbers in imagined matrix); recitation of numbers, days, or months backwards; backward spelling; storytelling; memorization of numbers, words or objects; and description of opposite direction of actions. In the variable priority instructional set, outcome data on task performance confirmed that the patient was prioritizing on the task as directed.

Silsupadol et al121 also used four laboratory dual-task outcome measures during walking (narrow path walking and obstacle crossing each combined with counting backward by threes and a tone discrimination task) to judge the effects of intervention pre- and post-intervention. Cognitive task accuracy and measurement of mediolateral center of mass displacement during the dual-task conditions were measured. In addition, a clinical test, the TUG with concurrent simple addition/subtraction was performed.

Balance improved for all patients after 4 weeks of three times weekly training. All patients improved in single- and dual-task performance of the TUG, but those who had trained in dual-task conditions showed greater improvements in the dual-task TUG. The patient who was trained in the variable priority instructional set also showed greater improvement on tasks that were not directly trained (laboratory measures), suggesting possible transfer of skills to novel dual-task conditions. These results are preliminary, but offer support for the use of dual-task training to improve dual-task performance. The relationship of these changes to future fall risk is as yet unclear, but will likely be the focus of ongoing research.

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Impairment and Task-Oriented Approaches for Rehabilitation

Rehabilitation is a complex process that consists of many components. As a means of understanding approaches that are in use, two treatment arms used in a randomized clinical trial for patients with TBI at the Defense and Veterans Brain Injury Center (DVBIC) are reviewed. The methods for this study were described by Vanderploeg et al.122 Therapists involved in this study selected two global ways of approaching rehabilitation when cognitive impairment was present, which they termed “cognitive-didactic” and “functional-experiential.” This dichotomy relates to explicit and implicit learning as well as impairment-based versus task-oriented intervention.

The cognitive-didactic approach was based on cognitive rehabilitation descriptions developed by neuropsychologists Sohlberg and Mateer123 with a significant focus on cognitive impairments. Specific cognitive and functional impairments (attention, memory, executive function, and pragmatics for communication) were targeted. Improved cognition was expected to translate to improved functional abilities. Therapy activities in this treatment arm were primarily didactic, teaching patients about their deficits, with a strong focus on meta-cognition (cognitive awareness of problems with attention). Patients were challenged by tasks of increasing difficulty and were encouraged to self-reflect on performance to facilitate problem solving for future success. This approach encouraged explicit learning about deficits as a way to improve awareness and promote strategy development.

Cognitive training specific to attention in the DVBIC study followed the Attention Process Training (APT) protocol also described by Sohlberg and Mateer.123 The goal of APT was to improve attention rather than encourage compensation. Structured activities were designed to increase the speed of information processing, amount of information processed, and complexity of attentional tasks. Clinicians determined the appropriate level of focus for attention training (based on the types reviewed previously: focused, sustained, selective, alternating, or divided). All therapists (occupational, physical, speech, and recreational) working with patients in this treatment arm devised activities requiring various types of attention. Similar tasks were grouped together to optimize practice of a particular type of attention.

An important element of APT was a method to score performance (accuracy, speed, or type of errors) so that progress could be observed. Patterns of error response were carefully evaluated to make decisions about increasing task difficulty. Each task was calibrated to encourage improvement by challenging without being too frustrating. Repetition was a key component of this process because cognitive activities must be practiced sufficiently to stimulate attentional processing.

In contrast, the functional-experiential approach was more of a task-oriented approach. This intervention focused on functional skills commonly impaired after brain injury and used group activities led by multiple disciplines to work on skills. Groups addressed current events, games/indoor recreation, sports, exercise, cooking, and prevocational activities. Treatment was conducted in natural environments by presenting tasks that required the use of a range of cognitive abilities, including attention. Therapists provided assistance, cues, and redirection for appropriate performance, but avoided problem-solving cues and open-ended questions.

Task complexity was gradually increased but only in so much as “errorless learning” occurred. The theory with this approach was that by practicing functional tasks in an errorless manner in a variety of contexts, implicit learning would be optimized.122,124 The assumption was that learning by doing would result in the elimination or remediation of cognitive impairments over time. Results of the intervention study have not been published.

This dichotomy, designed as a research paradigm, may falsely separate strategies used in neurorehabilitation. Both treatment approaches, the cognitive-didactic and the functional-experiential, may be used in a complementary way by therapists for patients with attention problems. This is convincingly illustrated by Tappan125 in her case report of a 16-year-old patient with attention deficits who was 6 months post–intracranial hemorrhage secondary to an arteriovenous malformation.

Consistent with the cognitive-didactic intervention for attention (APT), Tappan used assessments from the occupational therapist and speech-language pathologist to identify specific problems with different types of attention. During the PT examination, Tappan identified increased losses of balance and evidence of distraction in a distracting (versus nondistracting) environment during walking and the inability to perform balance measures (tandem gait, single-limb and tandem stance) as important baseline skills for improvement.

Through interdisciplinary collaboration, including cotreatments with occupational and speech therapy, the patient's therapy included walking and balance activities in a variety of conditions with gradually increased task and environmental challenges. Specific tasks were designed that required sustained, divided, alternating, and selective attention. Consistent with the functional-experiential approach, physical tasks were functional skills performed in real-life environments that challenged the patient with tasks pertinent for his or her daily mobility or recreational interests.

Balance task difficulty was progressed by decreasing sensory input (eyes closed), decreasing base of support, or incorporating dynamic activities (kicking a ball). Ambulation tasks progressed in difficulty by requiring the patient to carry a book bag (with increasing amount of weight) and requiring speed and direction changes during walking. Environmental manipulations included (1) increasing auditory input (background noise, conversation); (2) increasing environmental obstacles; (3) changing surface conditions; and (4) adding motion to the environment (perturbations, other people, escalators).

Consistent with the cognitive-didactic APT approach, attention tasks were monitored for errors. Distractions and losses of balance were recorded. Summary extrinsic feedback was provided for blocks of trials to describe both knowledge of results (number of balance losses) and knowledge of performance (reasons for loss of balance, eg, after looking at a distraction). Bandwidth extrinsic feedback was provided to the patient if safety appeared to be a concern during task performance. The effects of attentional problems on functional performance were emphasized to build awareness. As therapy progressed, the patient verbalized intrinsic awareness of how attention problems affected his or her safety and mobility. This type of insight provided an avenue for problem solving to prevent risky situations in the future. Once a task combination was performed without loss of balance, difficulty was increased by manipulating the task or environmental demands. This progression based on error-free performance is similar to the errorless learning principle described in the functional-experiential intervention from the DVBIC study.122

Tappan's intervention also included trunk and lower extremity strengthening activities designed as a home program, endurance training on a stationary bike and treadmill, and patient/family education in addition to therapy sessions that focused on attention during mobility. Following intervention (three times weekly for 11 weeks), the patient improved substantially in balance ability so that he or she was able to tandem walk (20 ft), could stand on one foot as long as 20 seconds, could walk and talk at the same time (a negative SWWT test), and could walk in community environments without balance loss. Although the mechanisms for improvement are not discernible from the case report, the systematic application of training principles is instructive for current practice and future research that addresses intervention to improve attention and mobility.

PT intervention appears inclined toward a task-oriented approach, supported by a recent review of the effects of PT on outcomes after stroke that advocates task-oriented intervention because of small to large effect sizes associated with training for locomotor recovery and upper extremity use.126 This tendency is somewhat in contrast with recommendations from systematic review for cognitive rehabilitation, which advocates intervention that directly addresses cognitive impairment to influence function.127,128 Tappan's case report is an example of how these two approaches may be effectively combined. Functional tasks can be practiced with analysis of the role of cognitive and motor impairments play in limiting functional independence.

Further investigation of these differing priorities in therapy activities is necessary to clearly direct practice and may help elucidate the “active ingredients”129 necessary to improve function when attention problems are manifest after ABI.

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CONCLUSION

Therapists choose activities that are consistent with a patient's current abilities but also present appropriate challenges to work toward therapy goals. In some cases, attention impairments may necessitate restricted activity or reduced environmental challenge to maintain safety or optimize therapy activity. As motor activity becomes more automatic in less demanding environmental conditions, additional distractions and environmental challenges can be added systematically. A structured approach to monitoring errors in performance of motor and cognitive tasks can guide decision making for when to increase task difficulty.

Patient's long-term goals typically target environments and roles that a patient is expected to resume. The use of dual- or multiple-task conditions simulates real life so that patients can learn strategies to attend to safety even with environmental distractions. Therapists can also use more challenging activities to identify situations that may need to be avoided. Therapists only need to consider typical demands of a usual day in the life of their patients to devise a range of treatment activities that require differing types of attention, with a variety of motor and cognitive skills. Activity-based exercise programs that are beneficial for health maintenance such as Tai Chi, dancing, and weight training often involve multiple task demands. Recreational sport activities also provide many possibilities for dual- or multiple- task performance.

Currently, there is limited evidence to guide implementation of treatment to address attention as part of intervention. Examples from the literature demonstrate a process of manipulating task and environment demands to gradually challenge patients. The ability to generalize novel dual-task conditions to real life has not been demonstrated for patients with neurologic involvement, so choosing therapy activities that are closer to real life is a reasonable approach, including combinations of motor tasks (walking and carrying items, walking while dialing a cell phone) and combinations of motor tasks with other cognitive tasks (conversation, list making, way finding).

Undoubtedly additional study of patients who have neurologic involvement is necessary to understand how attention and allocation of attention affect mobility and safety. As knowledge of the extent and nature of these problems expands, appropriate intervention strategies should also become evident.

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Keywords:

divided attention; brain injury; stroke

© 2007 Neurology Section, APTA

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Adults With Diabetic Peripheral Neuropathy Exhibit Impairments in Multitasking and Other Executive Functions

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