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

• Published in: NeuroImage (Orlando, Fla.) Vol. 189; pp. 745 - 754
• Main Authors: Wagshul, Mark E., Lucas, Melanie, Ye, Kenny, Izzetoglu, Meltem, Holtzer, Roee
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 01.04.2019; Elsevier Limited
• Subjects: Aged; Aged, 80 and over; Aging; Aging - pathology; Aging - physiology; Brain aging; Cognitive ability; Cohort Studies; Executive function; Executive Function - physiology; Female; fNIRS; Frontal lobe; Frontal Lobe - diagnostic imaging; Frontal Lobe - pathology; Frontal Lobe - physiology; Functional Neuroimaging - methods; Gait; Gray Matter - diagnostic imaging; Gray Matter - pathology; Gray Matter - physiopathology; Grey matter volume; Hemoglobin; Humans; Information sharing; Infrared spectroscopy; Magnetic resonance imaging; Magnetic Resonance Imaging - methods; Male; Motor activity; Multimodal Imaging; Neuroimaging; Neuroimaging - methods; Older people; Spectroscopy, Near-Infrared - methods; Studies; Substantia grisea; Velocity; Walking; Walking - physiology; Executive function; NP; fNIRS; Gait; Motor activity; DTW; PFC; LMM; Brain aging; GMV; GHS; RBANS; Grey matter volume; STW
• ISSN: 1053-8119; 1095-9572; 1095-9572
• DOI: 10.1016/j.neuroimage.2019.01.045

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. [Display omitted] •The relationship of frontal activity during walking to grey matter volume in aging was explored.•Frontal lobe volumetrics and fNIRS-oxyhemoglobin assessed during walking were measured.•Lower frontal grey matter volume was associated with increased frontal lobe activity.•Grey matter loss in aging may result in inefficient activation of frontal circuits while walking.