Inefficient frontal and parietal brain activation during dual-task walking in a virtual environment in older adults

Abstract

Walking while performing an additional cognitive task (dual-task walking; DT walking) is a common yet highly demanding behavior in daily life. Previous neuroimaging studies have shown that performance declines from single-task (ST) to DT conditions are accompanied by increased prefrontal cortex (PFC) activity. This increment is particularly pronounced in older adults and has been explained either by compensation, dedifferentiation, or inefficient task processing in fronto-parietal circuits. However, there is only limited evidence for the hypothesized fronto-parietal activity changes measured under real-life conditions such as walking. In this study, we therefore assessed brain activity in PFC and parietal lobe (PL), to investigate whether higher PFC activation during DT walking in older adults is related to compensation, dedifferentiation, or neural inefficiency. Fifty-six healthy older adults (69.11 ± 4.19 years, 30 female) completed three tasks (treadmill walking at 1 m/s, Stroop task, Serial 3's task) under ST and DT conditions (Walking + Stroop, Walking + Serial 3's), and a baseline standing task. Behavioral outcomes were step time variability (Walking), Balance Integration Score BIS (Stroop), and number of correct calculations S3_corr (Serial 3's). Brain activity was measured using functional near-infrared spectroscopy (fNIRS) over ventrolateral and dorsolateral PFC (vlPFC, dlPFC) and inferior and superior PL (iPL, sPL). Neurophysiological outcome measures were oxygenated (HbO₂) and deoxygenated hemoglobin (HbR). Linear mixed models with follow-up estimated marginal means contrasts were applied to investigate region-specific upregulations of brain activation from ST to DT conditions. Furthermore, the relationships of DT-specific activations across all brain regions was analyzed as well as the relationship between changes in brain activation and changes in behavioral performance from ST to DT. Data indicated the expected upregulation from ST to DT and that DT-related upregulation was more pronounced in PFC (particularly in vlPFC) than in PL regions. Activation increases from ST to DT were positively correlated between all brain regions, and higher brain activation changes predicted higher declines in behavioral performance from ST to DT. Results were largely consistent for both DTs (Stroop and Serial 3's). These findings more likely suggest neural inefficiency and dedifferentiation in PFC and PL rather than fronto-parietal compensation during DT walking in older adults. Findings have implications for interpreting and promoting efficacy of long-term interventions to improve DT walking in older persons.

Keywords: Cognitive aging; Compensation & dedifferentiation; Dual-Task costs; Elderly; Multitasking; Virtual reality; fNIRS.