Dual‐task balance control reveals cerebrovascular–behavioral relationships in older adults resistant to cognitive decline

Age-related decline in cerebrovascular function is linked to cognitive dysfunction.1 Cognitive dual-task interference (DTI) in balance control is well-known clinically and emerging as a key risk factor for dementia and falls.2-4 Links between cerebral blood flow, white matter hyperintensities, and dual-task performance have been found under pathologic conditions (e.g., diabetes, poststroke).5, 6 Physically-active older adults show an attenuated decline in cerebral blood flow compared to their sedentary peers, potentially due to exercise effects to reduce vascular stiffness and promote angiogenesis.7 However, whether variance in neurotypical age-related changes in the cerebrovascular system function plays a role in the development of cognitive-balance dual-tasking are less clear. Here, we tested the hypothesis that maintaining greater cerebral blood flow velocity (CBFv), measured clinically using transcranial Doppler ultrasound, supports dual-task cognitive and balance function in older adults. We also tested the relationship between CBFv and older adults' prioritization of balance versus cognitive performance under dual-task conditions, which has been associated with age-related disease.2, 3 In an exploratory analysis, we tested the effect of advanced age on the relationship between CBFv and cognitive-balance DTI. Community-dwelling, cognitively normal participants (76 ± 4 years; n = 30) completed clinical balance/cognitive testing under single-task and dual-task conditions. Balance performance was assessed as the total distance traversed during a challenging beam walking task. Cognitive performance was assessed as response time during a working memory n-back test. Resting CBFv of the middle cerebral artery was measured using transcranial Doppler ultrasound (Supplementary Text S1). We tested whether CBFv was associated with single-task and DTI and prioritization of balance and cognitive performance and the effects of using multiple linear regression analyses (detailed in Supplementary Text S1). During single-tasking, higher CBFv was associated with higher balance function, while no relationship was observed for cognitive performance. During dual-tasking, CBFv was associated with DTI across domains of balance and cognition; for cognitive DTI, this effect was driven by individuals ≥75 years (Figure 1; Supplementary Text S1). Individuals ≥75 years exhibited greater cognitive DTI, yet achieved similar balance DTI compared with those <75. Regardless of age, participants with higher CBFv demonstrated greater dual-task prioritization of balance control over cognitive performance (Figure 2). Notably, individuals ≥75 years tended to ambulate at faster speeds on average during beam walking (25% faster, single-tasking; 13% faster, dual-tasking), but this difference was not statistically significant (Supplementary Text S1). These results support a link between cerebrovascular system function and cognitive-balance dual-task behavior in cognitively normal older adults. This cerebrovascular–behavioral link may emerge earlier in brain aging processes affecting balance control compared with cognition. Further, cerebrovascular function may support people's ability to prioritize balance in the face of competing attentional demands. Challenging balance revealed cerebrovascular–behavior relationships, which were not present during single-task cognitive performance. The emergence of cerebrovascular–cognitive relationships under dual-task conditions was exclusive to individuals ≥75 years (Figure 1C), suggesting that older adults exhibit less cognitive resilience to the unique neuromotor challenge presented by balance and mobility.8-10 The presence of these relationships during active balance control could be due to increased cardiovascular and cerebrovascular system requirements for the blood supply necessary for active muscle contraction. From a clinical perspective, these results support the use of balance testing to expose early biomarkers of behavioral dysfunction and associated cerebrovascular factors that can be therapeutically targeted. The investigation of a wider range of ages will help elucidate the nature of the interactive effects of aging on the relationship between cerebrovascular function and DTI. Alteration of cognitive-motor prioritization is a marker of disease state, in which dual-task costs to mobility shift to exceed those to cognition.2, 3 As expected, individuals ≥75 years demonstrated compromised cognitive DTI, yet, surprisingly, showed comparable balance DTI to their younger counterparts (Figure 2). Further, individuals with higher CBFv showed a greater prioritization of balance over cognition, irrespective of age (Figure 2C), implicating that maintaining cerebrovascular function may support older adults' ability to prioritize balance over cognition during simultaneous demands for limited attentional resources. An interesting and unexpected finding was that the older group tended to ambulate faster during beam walking, which could be due to the study selection of older adults resistant to cognitive decline. These older individuals may also show exceptional resilience to the normal declines expected for walking speed and balance control, for which cerebrovascular health may serve a neuroprotective role as supported by the present results. Our findings in a model of healthy aging suggest that early clinical manifestations of cognitive-motor dual-task dysfunction could be influenced by cerebrovascular system changes. Cerebrovascular health could be an early therapeutic target to positively influence the trajectory of cognitive DTI with aging. Jacqueline A. Palmer conceived of the present research question and designed this study. Jacqueline A. Palmer and Sandra A. Billinger obtained funding to support this study. Jacqueline A. Palmer and Emily M. Hazen collected and analyzed the data. Sandra A. Billinger, Emily M. Hazen, and the KU Alzheimer's Disease Research Center contributed to recruitment. Jacqueline A. Palmer constructed the figures and the first draft of this manuscript. Sandra A. Billinger contributed the analysis tools and expertise for interpreting cerebrovascular data. All authors discussed the results and contributed to the final manuscript. The authors have no conflicts of interest to disclose. This work was supported by the National Institute on Aging of the National Institutes of Health [K99AG075255 (JP)] and [P30 AG072973 (SB)] and the Georgia Holland Endowment Fund. The content of this publication is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health or any other funding agency. This research was supported by the Extramural Research Program of the National Institutes of Health. Supplemental Text S1. Detailed Materials and Methods. Supplemental Table S1. Participant characteristics. Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. 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