Prefrontal cortex activation during dual-task walking in older adults is moderated by thickness of several cortical regions

Abstract

healthy community-dwelling older adults, whose cortical thickness was measured via MRI. HbO 2 levels in the PFC, measured via fNIRS, were assessed during active walking under STW and DTW conditions. Statistical analyses were adjusted for demographics and behavioral performance. Linear mixed-effects models revealed that the increase in HbO 2 from STW to DTW was moderated by cortical thickness in several regions. Specifically, thinner cortex in specific regions of the frontal, parietal, temporal, and occipital lobes, cingulate cortex, and insula was associated with greater increases in HbO 2 levels from single to dual-task walking. In conclusion, participants with thinner cortex in regions implicated in higher order control of walking employed greater neural resources, as measured by increased HbO 2 , in the PFC during DTW, without demonstrating benefits to behavioral performance. To our knowledge, this is the first study to examine cortical thickness as a marker of neural inefficiency during active walking.

Differential Relationships Between Brain Structure and Dual Task Walking in Young and Older Adults

“…This also results in a stronger relationship between temporal lobe structure and dual task walking, which only emerges in older age when these neural resources start to become limited. This interpretation fits with a recent report of an association between lower cortical thickness and greater increases in prefrontal oxygenation from single to dual task walking, with no effect on performance (Ross et al, 2021 ). The study authors suggested that older adults with the poorest neural resources (i.e., the thinnest cortex) also required the most compensation from alternative brain regions (i.e., the greatest increases in prefrontal oxygenation) to maintain performance.…”

“…We did not identify any statistically significant age group differences in the relationship between the DTcost of gait speed or variability and regional gray matter volume. While extensive previous literature has examined relationships of single task overground walking with gray matter and cerebellar volume (e.g., Rosano et al, 2007 ; Dumurgier et al, 2012 ; Callisaya et al, 2013 ; Beauchet et al, 2015 ; Demnitz et al, 2017 ), comparatively less work has examined such relationships with dual task walking (Allali et al, 2019 ; Lucas et al, 2019 ; Tripathi et al, 2019 ; Wagshul et al, 2019 ; Ross et al, 2021 ). Further, these studies had methodological differences from our work (e.g., they used an alphabet task instead of serial 7s as the cognitive task).…”

“…We identified several age differences in brain-behavior relationships for two surface metrics: cortical thickness and sulcal depth. Only a few previous studies have examined relationships between cortical thickness and dual task walking in aging (Maidan et al, 2021;Ross et al, 2021), and, to our knowledge, no prior literature has examined sulcal depth in relation to dual task walking in aging. In the present work, we identified a relationship between thinner temporal cortex and greater increases in step time variability from single to dual task walking for older adults.…”

“…There are clear cortical contributions to the control of walking (Miyai et al, 2001 ; Petersen et al, 2012 ; Allali et al, 2014 ; Koenraadt et al, 2014 ; Takakusaki, 2017 ). Thus, poorer dual task walking performance in older age has been attributed, at least in part, to age-related brain atrophy (Allali et al, 2019 ; Lucas et al, 2019 ; Ross et al, 2021 ). A large body of literature suggests that age-related structural brain atrophy occurs in an anterior-to-posterior pattern, with the frontal cortices atrophying earlier and faster than other regions of the brain (e.g., Salat et al, 2004 ; Fjell et al, 2009a ; Thambisetty et al, 2010 ; Lemaitre et al, 2012 ).…”

“…Two previous studies found associations between greater gait slowing during dual task walking in older adults and lower gray matter volume in the middle frontal gyrus (Allali et al, 2019 ), medial prefrontal and cingulate cortices, and thalamus (Tripathi et al, 2019 ). Further, several studies found that older adults who showed a greater increase in prefrontal cortex oxygenation from single to dual task walking also had lower white matter fractional anisotropy (averaged across the whole white matter mask; Lucas et al, 2019 ), lower gray matter volume within the frontal lobe (Wagshul et al, 2019 ), and reduced thickness across the cortex (Ross et al, 2021 ). These imaging metrics were not related to faster dual task walking, though, suggesting that the observed increases in prefrontal cortex activity represented compensation to maintain walking performance, despite atrophying brain structure.…”