Paradoxical improvement of cognitive control in older adults under dual-task walking conditions is associated with more flexible reallocation of neural resources: A Mobile Brain-Body Imaging (MoBI) study

Abstract

Combining walking with a demanding cognitive task is traditionally expected to elicit decrements in gait and/or cognitive task performance. However, it was recently shown that, in a cohort of young adults, most participants paradoxically improved performance when walking was added to performance of a Go/NoGo response inhibition task. The present study aims to extend these previous findings to an older adult cohort, to investigate whether this paradoxical improvement when dual-tasking is observed in healthy older adults. Mobile Brain/Body Imaging (MoBI) was used to record electroencephalographic (EEG) activity, three-dimensional (3D) gait kinematics and behavioral responses in the Go/NoGo task, during sitting or walking on a treadmill, in 34 young adults and 37 older adults. Increased response accuracy during walking, independent of age, was found to correlate with slower responses to stimuli and with walking-related EEG amplitude modulations over latencies and topographies related to the cognitive component of inhibition. On the other hand, aging, independent of response accuracy during walking, was found to correlate with slower treadmill walking speeds and attenuation in walking-related EEG amplitude modulations over latencies and topographies associated with the motor component of inhibition. Older adults whose response accuracy improved during walking manifested neural signatures of both behavioral improvement and aging, suggesting that their flexibility in reallocating neural resources while walking might be maintained for the cognitive but not for the motor inhibitory component. These distinct neural signatures of aging and behavior can potentially be used to identify super-agers, or individuals at risk for cognitive decline due to aging or neurodegenerative disease.

Reduced Proactive and Reactive Cognitive Flexibility in Older Adults Underlies Performance Costs During Dual-Task Walking: A Mobile Brain/Body Imaging (MoBI) Study

“…Lower amplitude alterations to anticipatory and reactive processes, coupled with deteriorating behavioral performance as demands increased, may reflect reduced cognitive flexibility in older adults. These results replicated, and expanded upon the findings of our previous studies (Malcolm et al, 2015;Patelaki, Foxe, Mantel, et al, 2023;Patelaki et al, 2022;Patelaki, Foxe, McFerren, & Freedman, 2023;Richardson et al, 2022).…”

“…Dual-task effects on performance were categorized into "improvement", "no change", or "cost" according to the procedure used by Patelaki and colleagues (Patelaki, Foxe, Mantel, et al, 2023;Patelaki et al, 2022). Walking-minus-sitting d' values and response times for each participant were defined as dual-task improvement or cost if they fell outside the 95% confidence interval of the normal distribution centered around a mean of zero and with a standard deviation equal to the variance of the entire cohort of younger and older adults.…”

“…Delayed and diminished accentuation of control processes in the context of larger dualtask performance costs were interpreted as neurophysiological indicators of reduced flexibility in the control processes of older adults. Lower amplitude accentuation during dual-task conditions may be a feature of reduced adaptation to cognitive-motor demands irrespective of age (Patelaki, Foxe, Mantel, Kassis, & Freedman, 2023;Patelaki et al, 2022). Among the likely many factors which contribute to successful cognitive-motor adaptation, preparation in advance of demanding cognitive events is characteristically reduced within the reactive modes of control which predominate in older adults (Braver, 2012;Gajewski et al, 2018;Kopp et al, 2014).…”

Functional near‐infrared spectroscopy evidence of cognitive–motor interference in different dual tasks

“…As a result, walking speed during DTs decreased when compared with walking alone, which is consistent with previous research findings (Doi et al, 2013; Hall et al, 2011; Mirelman et al, 2014). However, some studies have shown either maintained or improved gait integrity and cognitive performance during DT walking (De Sanctis et al, 2014; Fraser et al, 2016; Hamacher et al, 2019; Hausdorff, 2005; Patelaki et al, 2023, 2023; Richardson et al, 2022); these findings were believed to be related to neural circuit flexibility compensation (Richardson et al, 2022).…”

“…Further research has indicated that a concurrent cognitive task may reduce the input from high‐level cognitive processes for the control of gait, thus resulting in deterioration in walking performance (Mirelman et al, 2014; Wrightson et al, 2016). However, some studies have shown either maintained or improved gait integrity and cognitive performance during DT walking (De Sanctis et al, 2014; Fraser et al, 2016; Hamacher et al, 2019; Hausdorff, 2005; Patelaki et al, 2023, 2023; Richardson et al, 2022). Assessing gait and cognitive interference simultaneously can shed light on the possible influence of task prioritization strategies on DT performance (Li et al, 2014).…”