Reduced Vestibular Function is Associated with Cortical Surface Shape Changes in the Frontal Cortex

Abstract

Aging-associated decline in peripheral vestibular function is linked to deficits in executive ability, self-motion perception, and motor planning and execution. While these behaviors are known to rely on the sensorimotor and frontal cortices, the precise pathways involving the frontal and sensorimotor cortices in these vestibular-associated behaviors are unknown. To fill this knowledge gap, this cross-sectional study investigates the relationship between age-related variation in vestibular function and surface shape alterations of the frontal and sensorimotor cortices, considering age, intracranial volume, and sex. Data from 117 participants aged 60+ from the Baltimore Longitudinal Study of Aging, who underwent end-organ-specific vestibular tests (cVEMP for the saccule, oVEMP for the utricle, and vHIT for the horizontal canal) and T1-weighted MRI scans on the same visit, were analyzed. We examined ten brain structures in the putative "vestibular cortex": the middle-superior part of the prefrontal cortex (SFG_PFC), frontal pole (SFG_pole), and posterior pars of the superior frontal gyrus (SFG), the dorsal prefrontal cortex and posterior pars of middle frontal gyrus (MFG_DPFC, MFG), the pars opercularis, pars triangularis, and pars orbitalis of the inferior frontal gyrus, as well as the precentral gyrus and postcentral gyrus (PoCG) of the sensorimotor cortex. For each region of interest (ROI), shape descriptors were estimated as local compressions and expansions of the population average ROI surface using surface LDDMM. Shape descriptors were linearly regressed onto standardized vestibular variables, age, intracranial volume, and sex. Lower utricular function was linked with surface compression in the left MFG and expansion in the bilateral SFG_pole and left SFG. Reduced canal function was associated with surface compression in the right SFG_PFC and SFG_pole and left SFG. Both reduced saccular and utricular function correlated with surface compression in the posterior medial part of the left MFG. Our findings illuminate the complexity of the relationship between vestibular function and the morphology of the frontal and sensorimotor cortices in aging. Improved understanding of these relationships could help in developing interventions to enhance quality of life in aging and populations with cognitive impairment.