Multi-modal neuroimaging of dual-task walking: Structural MRI and fNIRS analysis reveals prefrontal grey matter volume moderation of brain activation in older adults

• DOI: 10.1016/j.neuroimage.2019.01.045
• Publication Date: 2019-01-30T17:35:12Z
• Authors: Mark E. Wagshul; Melanie Lucas; Kenny Ye; Meltem Izzetoglu; Roee Holtzer
• Keywords: Aged, 80 and over; Male; Aging; Spectroscopy, Near-Infrared; Functional Neuroimaging; Neuroimaging; Walking; Magnetic Resonance Imaging; Multimodal Imaging; Frontal Lobe; Cohort Studies; Executive Function; 03 medical and health sciences; 0302 clinical medicine; Humans; Female; Gray Matter; Aged

It has been well established over the last two decades that walking is not merely an automatic, motoric activity; it also utilizes executive function circuits, which play an increasingly important role in walking for older people and those with mobility and cognitive deficits. Dual-task walking, such as walking while performing a cognitive task, is a necessary skill for everyday functioning, and has been shown to activate prefrontal lobe areas in healthy older people. Another well-established point in healthy aging is the loss of grey matter, and in particular loss of frontal lobe grey matter volume. However, the relationship between increased frontal lobe activity during dual-task walking and loss of frontal grey matter in healthy aging remains unknown. In the current study, we combined oxygenated hemoglobin (HbO2) data from functional near-infrared spectroscopy (fNIRS), taken during dual-task walking, with structural MRI volumetrics in a cohort of healthy older subjects to identify this relationship. We studied fifty-five relatively healthy, older participants (≥65 years) during two separate sessions: fNIRS to measure HbO2 changes between single-task (i.e., normal walking) and dual-task walking-while-talking, and high-resolution, structural MRI to measure frontal lobe grey matter volumes. Linear mixed effects modeling was utilized to determine the moderation effect of grey matter volume on the change in prefrontal oxygenated hemoglobin between the two walking tasks, while controlling for covariates including task performance. We found a highly significant interaction effect between frontal grey matter volume and task on HbO2 levels (p < 0.0001). Specifically, increased HbO2 levels during dual-task compared to single-task walking were associated with reduced frontal grey matter volume. Regional analysis identified bilateral superior and rostral middle gyri as the primary areas driving these results. The findings provide support for the concept of neural inefficiency: in the absence of behavioral gains, grey matter loss in relatively healthy, older individuals leads to over-activation of frontal lobe during a cognitively demanding walking task with established clinical and predictive utility.