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The Journals of Gerontology Series A: Biological Sciences and Medical Sciences 63:1325-1328 (2008)
© 2008 The Gerontological Society of America


SPECIAL SECTION

Guest Editorial

Linking Thinking, Walking, and Falling

Neil B. Alexander and Jeffrey M. Hausdorff

1 Division of Geriatric Medicine, Department of Internal Medicine, University of Michigan, and VA Ann Arbor Health Care System GRECC, Ann Arbor.
2 Department of Neurology, Tel Aviv Sourasky Medical Center; Sackler Faculty of Medicine, Tel Aviv University, Israel; and Division on Aging, Harvard Medical School, Boston, Massachusetts.

Address correspondence to Neil B. Alexander, MD, VA Ann Arbor Health Care System GRECC, 2215 Fuller Rd. (11G), Ann Arbor, MI 48105-2300. E-mail: nalexand{at}umich.edu

THE link between cognition, gait, and the potential for falls is being increasingly recognized. In this special section of the Journal, a number of experts present new data that further explore the mechanisms underlying this link.


    SIGNIFICANCE
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 Significance
 Contributions of Specific...
 Future Research
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Disorders of gait are increasingly linked to poor outcomes, such as an increased risk of institutionalization and death (1). Gait disorders also predict future decline in cognitive function. Nondemented participants with clinically abnormal gait (particularly unsteady, frontal, or hemiparetic gait) and followed for approximately 7 years were at higher risk of developing non-Alzheimer's, particularly vascular, dementia (2). Of note, at baseline, those with abnormal gait may not have met criteria for dementia, but already had abnormalities in neuropsychological function, such as in visual–perceptual processing and language skills. In a subsequent analysis, quantitative gait analyses in nondemented participants predicted cognitive decline and dementia in a 2-year follow-up (3). In healthy older adults followed for approximately 4 years, slowed gait speed is a predictor of mild cognitive impairment (MCI), independent of memory loss (4).

Cognitive impairment has long been noted to associate with disorders of balance and gait, and falls in particular. Demented (particularly Alzheimer's disease, AD) individuals have slower gait speed and greater step-to-step variability (5,6), larger postural sway paths (5), poorer ability to maintain stable stance in response to perturbations (such as a reduced support surface) (6), and poorer performance on simple timed balance tests (7). Compared with age-matched controls, patients with AD land with their feet more closely to an obstacle after crossing it, and are more likely to contact the obstacle in their path (6), behaviors that may place them at greater risk for falls. More importantly, patients with AD are at particular risk for falls. At initial visit, nearly one third of an AD group reported a history of falls since the onset of their dementing illness (8). Another prospective series found that AD patients, when compared to cognitively intact older adults, had a three-fold increase in falls causing fracture or hospitalization and that these falls were associated with institutionalization (9). A two-fold increase in risk for falls in demented versus nondemented nursing home residents has also been reported (10). Even patients with MCI are thought to have small decrements in timed balance tasks (7) and an increased fall risk (11). Further, an 8-year prospective study demonstrated that Mini-Mental State Examination and verbal reasoning at baseline predicted the rate of falling (12). Within individuals, declines in verbal ability, processing speed, and immediate memory are associated with increases in rates of falling and fall risk. Thus, alterations in walking abilities apparently predict and, to some extent, may predate the clinical appearance of cognitive changes. At the same time, cognitive alterations apparently are associated with alterations in postural control and gait and are predictive of falls.


    CONTRIBUTIONS OF SPECIFIC COGNITIVE FACTORS
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 Significance
 Contributions of Specific...
 Future Research
 References
 
Declines in attention, psychomotor processing, problem-solving, and awareness of self and surroundings apparently have the biggest impact on postural control, gait, and falls. Executive function measures are thought to be particularly good predictors of falls (13,42) and contribute to disruptions of gait and balance (14,15). A common test of attention and psychomotor processing speed, the Trail Making Test B (TMT-B), associates with injurious falls (16) as well as with physical performance and self-reported disability (17,18). Moreover, successful avoidance of an obstacle can be predicted by measures of problem solving, response inhibition, general anxiety, and variability in attention (19). Impairment in executive function may be particularly important in certain disease groups, that is, inattention predicts falls in patients with Parkinson's disease (20) and dual-task decrements in patients with AD (14,21). Furthermore, in response to a single dose of methylphenidate, gait parameters improve, possibly via an effect on executive function (22).

Decrements in attention and executive function likely influence postural control and gait performance under conditions where a subject must also perform an accompanying task of varying cognitive load (i.e., two tasks at once, hence the term "dual task"). According to one theory, in a "divided attention" or "dual task" situation, increasing the attentional demand of a cognitive task will decrease the resources available to perform a postural control or gait task; postural control or gait performance will consequently decline. While questions remain about the predictive value of this relationship, dual-task performance has been linked to an increased risk of falls based on walking performance while performing a simultaneous cognitive (dual) task. The risk of falls, measured prospectively, increases in those who: 1) stop walking while talking (23), 2) slow down their timed up and go performance while carrying a glass of water (24), and 3) slow their walking while performing a series of verbal cognitive tasks (reciting the alphabet consecutively and alternately) (25). Of note, the simplest test, stops walking while talking, may be only useful in those who are very impaired in their ability to walk while performing another task (26).

Articles in this special section focus on the apparent influence of cognitive function, especially executive function, as a critical contributor to walking, particularly under conditions when the gait-related task requires a higher level of cognitive input. As is true with much of the previous literature, one aspect of executive function, dual-task performance, is used to further understand the contribution of cognition to mobility performance in healthy older adults and is repeatedly revealed to be a critical component in the link between gait and cognitive function. Kelly and colleagues confirm that, with more challenging gait tasks such as walking on a narrow base, walking speed declines with dual-task performance (27). Dual-task performance also affects key aspects of walking such as gait variability, and performance on typical tests of executive function are associated with these dual-task functional gait decrements in healthy aging, although it appears that the factors that contribute to dual-tasking are multifactorial and not yet fully elucidated (28).

The influence of executive function on gait and balance can be seen beyond healthy older adults and in more diverse older adult community dwellers and patient groups with cognitive impairments. Van Iersel and colleagues found that dual-task performance affects gait variability and mediolateral trunk sway, and that executive function, and not memory function, associates with these performance decrements (29). A commonly used Trail Making Test (TMT) was embedded in a walkway by Persad and colleagues (Walking or W-TMT), creating a stepping accuracy test that might simulate the traversing of challenging terrain such as uneven or slippery surfaces and thereby present a dual task with cognitive demand embedded in the walkway (30). In their article, patients with AD and MCI featuring memory and executive function impairments took longer to traverse the walkway than normal controls or patients with MCI with only memory impairment, specifically on the more cognitively demanding W-TMT-B. As might be expected, slower performance on W-TMT-B associates with declines in executive function and not other neuropsychological aspects such as memory.

Finally, in studying navigation, an important ability that may be lost with cognitive impairment, Sanders and colleagues developed a novel mobility-related test embedded with cognitive demand (31). As with many of the studies above, the most important contributor to navigation skill in relatively healthy older adults was executive function.

Other articles provide additional insight into the underlying features of these dual-task effects. Siu and colleagues report that, compared to young controls, healthy older adults are less able to deal with a dual-task paradigm, that is, they are less able to allocate attention to a typical executive function task, the Stroop test, when required to avoid an obstacle (32). In Zettel and colleagues (33), participants perform a visual tracking task and then simultaneously step rapidly in response to an unexpected platform perturbation. Reallocation of attentional resources may have a direct impact on initial stance postural stabilization prior to the step in older but not younger adults. We now have data supporting what clinicians have suspected all along; when we are distracted or attempt to do something that diverts attention from walking or stepping, both walking performance and postural stability can be affected.

A number of studies have now linked alterations in brain structure to gait disorders and falls. Increases in cerebral white matter hyperintensities have been prospectively associated with functional balance and gait abnormalities and falls (34,35). The link between these structural changes, gait, and cognition has also been proposed. Both executive function and slow gait speed, independent of these changes and alone or in combination, increase mortality and disability (36). In the present section, Rosano and colleagues evaluate how focal brain atrophy on MRI might relate to quantitative gait parameters. Shorter steps and longer double support times associate with smaller sensorimotor and frontoparietal regions within the motor, visuospatial, and cognitive processing speed domains (37).


    FUTURE RESEARCH
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Future research should further explore the mechanisms underlying dual-task effects occurring in both healthy and impaired older adults. How much attention is required for different cognitive and mobility tasks? How much attention diversion is necessary to actually lose balance or, more importantly, how much residual attention is needed to avoid loss of balance? Does the increase in task complexity, either cognitive or mobility, result in predictable linear decrements in performance? How does prioritization of the task affect the outcome, that is, is safe stance and walking always prioritized to the detriment of cognitive response? Prioritization may not be a major issue for relatively healthy older adults on relatively easy mobility and cognitive tasks. Thus, the dual task effect may be minimal in healthy older adults with sufficient physical and cognitive reserves. Verghese found that participants who were told to prioritize walking and talking equally were less likely to slow down than those who prioritized talking over walking, but the differences were small and there was no effect on the cognitive measures (38).

Nevertheless, because of these prioritization and "reserves" issues, to properly understand the dual-task effects, future studies should simultaneously monitor both mobility as well as cognitive performance. Assessing the "cost" of the added cognitive task, as was done by Siu and colleagues, may be one effective approach to understanding the effect of simultaneous cognitive tasks on mobility (32).

The level of patient impairment and patients' awareness of their limitations must also be considered. Might a patient with impaired physical function who is appropriately aware of his or her limitations have minimal dual-task decrement because he or she maintains performance at a safe low level? Moreover, physical impairment may reach a low level such that cognition is needed just to monitor walking. Thus, a dual task may be very difficult, if not impossible, for a physically impaired older adults to perform (i.e., stops talking while walking). A situation of greater concern is that of the patient who is not aware of his or her limitations, and who is inappropriately focusing on simultaneous tasks when he or she should be focusing on his or her mobility or even walking speed (39). Even more critical is the cognitively impaired older adult who has difficulty in dual-task situations requiring monitoring of the environment for hazards. Decreased attention and judgment in a demented older adult may cause a lack of recognition of obstacles or hazards, an issue not yet addressed in the dual-task literature, which may be critical in fall causation in this population.

There should be some consideration of both the types of mobility and cognitive tasks and how they interact. Dual-task effects may depend on the task type (e.g., which cognitive domains are being taxed), complexity (i.e., the level of difficulty, for example, subtractions by 1s or subtractions by 7s), and the specifics of the instruction set (i.e., is one task implicitly given priority?). Distractors (or divided attention) might be more important in causing mobility disruptions (or falls) during the performance of a task that requires surveillance of an obstacle or hazard. Distractors might be more important when a more active, dynamic, larger intensity, more rapid motion is required such as during a rapid or longer step. Distractors might be more important when they occur on a certain critical portion of the gait cycle such as during weight shift. Once balance is lost, cognitive factors may be less important than musculoskeletal factors (such as muscle power), although it may be possible to alter late-stage fall responses via learned strategies. Still, it is likely that cognitive function takes on a more prominent role as gait slows and becomes less automatic.

Future research is also needed to better understand how structural brain pathophysiology underlies the contribution of cognition to mobility. The relationships between cognition, mobility, and possibly affect are now being considered (40), possibly through a unifying vascular disease etiology, a focus of a recent National Institute on Aging conference. One of the challenges to conducting this research, however, is that real-time imaging of the brain is difficult to perform during a simultaneous weight-bearing task, particularly while quantifying walking performance.

How cognition affects mobility and ultimately fall risk involves a number of factors beyond dual-task paradigms. One model of how neuropsychological function influences walking suggests that executive function may control behavior (e.g., walking), but the system is built upon a base of cognitive, physical, and affect/self-efficacy capacities, and then modulated by age and disease, the demands of the task, and the environment (41). Thus, future research may need to consider a more expansive model to more fully understand cognition and fall risk.

Future studies are needed to assess where and when cognitive function becomes more prominent in determining walking performance, particularly during more challenging walking activities, as well as the physiological substrates that link walking, thinking, and falling. A more complete understanding of this link should also, ultimately, enhance our ability to optimize treatment of impairments in cognitive function and walking and thus reduce the risk of falls among older adults.


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