Novel attentional gait index reveals a cognitive ability-related decline in gait automaticity during dual-task walking

IntroductionGait automaticity refers to the ability to walk with minimal recruitment of attentional networks typically mediated through the prefrontal cortex (PFC). Reduced gait automaticity (i.e., greater use of attentional resources during walking) is common with aging, contributing to an increase...

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Main Authors: Shuqi Liu, Andrea L. Rosso, Emma M. Baillargeon, Andrea M. Weinstein, Caterina Rosano, Gelsy Torres-Oviedo
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-01-01
Series:Frontiers in Aging Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fnagi.2023.1283376/full
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author Shuqi Liu
Shuqi Liu
Andrea L. Rosso
Emma M. Baillargeon
Andrea M. Weinstein
Caterina Rosano
Gelsy Torres-Oviedo
Gelsy Torres-Oviedo
author_facet Shuqi Liu
Shuqi Liu
Andrea L. Rosso
Emma M. Baillargeon
Andrea M. Weinstein
Caterina Rosano
Gelsy Torres-Oviedo
Gelsy Torres-Oviedo
author_sort Shuqi Liu
collection DOAJ
description IntroductionGait automaticity refers to the ability to walk with minimal recruitment of attentional networks typically mediated through the prefrontal cortex (PFC). Reduced gait automaticity (i.e., greater use of attentional resources during walking) is common with aging, contributing to an increased risk of falls and reduced quality of life. A common assessment of gait automaticity involves examining PFC activation using near-infrared spectroscopy (fNIRS) during dual-task (DT) paradigms, such as walking while performing a cognitive task. However, neither PFC activity nor task performance in isolation measures automaticity accurately. For example, greater PFC activation could be interpreted as worse gait automaticity when accompanied by poorer DT performance, but when accompanied by better DT performance, it could be seen as successful compensation. Thus, there is a need to incorporate behavioral performance and PFC measurements for a more comprehensive evaluation of gait automaticity. To address this need, we propose a novel attentional gait index as an analytical approach that combines changes in PFC activity with changes in DT performance to quantify automaticity, where a reduction in automaticity will be reflected as an increased need for attentional gait control (i.e., larger index).MethodsThe index was validated in 173 participants (≥65 y/o) who completed DTs with two levels of difficulty while PFC activation was recorded with fNIRS. The two DTs consisted of reciting every other letter of the alphabet while walking over either an even or uneven surface.ResultsAs DT difficulty increases, more participants showed the anticipated increase in the attentional control of gait (i.e., less automaticity) as measured by the novel index compared to PFC activation. Furthermore, when comparing across individuals, lower cognitive function was related to higher attentional gait index, but not PFC activation or DT performance.ConclusionThe proposed index better quantified the differences in attentional control of gait between tasks and individuals by providing a unified measure that includes both brain activation and performance. This new approach opens exciting possibilities to assess participant-specific deficits and compare rehabilitation outcomes from gait automaticity interventions.
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spelling doaj.art-cf5391ba4e6f4dd7960f0a6270c14a602024-01-11T05:08:17ZengFrontiers Media S.A.Frontiers in Aging Neuroscience1663-43652024-01-011510.3389/fnagi.2023.12833761283376Novel attentional gait index reveals a cognitive ability-related decline in gait automaticity during dual-task walkingShuqi Liu0Shuqi Liu1Andrea L. Rosso2Emma M. Baillargeon3Andrea M. Weinstein4Caterina Rosano5Gelsy Torres-Oviedo6Gelsy Torres-Oviedo7Sensorimotor Learning Laboratory, Department of Bioengineering, University of Pittsburgh, Pittsburgh, PA, United StatesCenter for the Neural Basis of Cognition, Pittsburgh, PA, United StatesDepartment of Epidemiology, University of Pittsburgh, Pittsburgh, PA, United StatesDepartment of Medicine, Division of Geriatric Medicine, University of Pittsburgh, Pittsburgh, PA, United StatesDepartment of Psychiatry, School of Medicine, University of Pittsburgh, Pittsburgh, PA, United StatesDepartment of Epidemiology, University of Pittsburgh, Pittsburgh, PA, United StatesSensorimotor Learning Laboratory, Department of Bioengineering, University of Pittsburgh, Pittsburgh, PA, United StatesCenter for the Neural Basis of Cognition, Pittsburgh, PA, United StatesIntroductionGait automaticity refers to the ability to walk with minimal recruitment of attentional networks typically mediated through the prefrontal cortex (PFC). Reduced gait automaticity (i.e., greater use of attentional resources during walking) is common with aging, contributing to an increased risk of falls and reduced quality of life. A common assessment of gait automaticity involves examining PFC activation using near-infrared spectroscopy (fNIRS) during dual-task (DT) paradigms, such as walking while performing a cognitive task. However, neither PFC activity nor task performance in isolation measures automaticity accurately. For example, greater PFC activation could be interpreted as worse gait automaticity when accompanied by poorer DT performance, but when accompanied by better DT performance, it could be seen as successful compensation. Thus, there is a need to incorporate behavioral performance and PFC measurements for a more comprehensive evaluation of gait automaticity. To address this need, we propose a novel attentional gait index as an analytical approach that combines changes in PFC activity with changes in DT performance to quantify automaticity, where a reduction in automaticity will be reflected as an increased need for attentional gait control (i.e., larger index).MethodsThe index was validated in 173 participants (≥65 y/o) who completed DTs with two levels of difficulty while PFC activation was recorded with fNIRS. The two DTs consisted of reciting every other letter of the alphabet while walking over either an even or uneven surface.ResultsAs DT difficulty increases, more participants showed the anticipated increase in the attentional control of gait (i.e., less automaticity) as measured by the novel index compared to PFC activation. Furthermore, when comparing across individuals, lower cognitive function was related to higher attentional gait index, but not PFC activation or DT performance.ConclusionThe proposed index better quantified the differences in attentional control of gait between tasks and individuals by providing a unified measure that includes both brain activation and performance. This new approach opens exciting possibilities to assess participant-specific deficits and compare rehabilitation outcomes from gait automaticity interventions.https://www.frontiersin.org/articles/10.3389/fnagi.2023.1283376/fullagingnear-infrared spectroscopylocomotioncommunity mobilitycognitionbrain imaging
spellingShingle Shuqi Liu
Shuqi Liu
Andrea L. Rosso
Emma M. Baillargeon
Andrea M. Weinstein
Caterina Rosano
Gelsy Torres-Oviedo
Gelsy Torres-Oviedo
Novel attentional gait index reveals a cognitive ability-related decline in gait automaticity during dual-task walking
Frontiers in Aging Neuroscience
aging
near-infrared spectroscopy
locomotion
community mobility
cognition
brain imaging
title Novel attentional gait index reveals a cognitive ability-related decline in gait automaticity during dual-task walking
title_full Novel attentional gait index reveals a cognitive ability-related decline in gait automaticity during dual-task walking
title_fullStr Novel attentional gait index reveals a cognitive ability-related decline in gait automaticity during dual-task walking
title_full_unstemmed Novel attentional gait index reveals a cognitive ability-related decline in gait automaticity during dual-task walking
title_short Novel attentional gait index reveals a cognitive ability-related decline in gait automaticity during dual-task walking
title_sort novel attentional gait index reveals a cognitive ability related decline in gait automaticity during dual task walking
topic aging
near-infrared spectroscopy
locomotion
community mobility
cognition
brain imaging
url https://www.frontiersin.org/articles/10.3389/fnagi.2023.1283376/full
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