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 behaviors and cognitive abilities that are known to rely on the sensorimotor and frontal cortices, but the precise neural pathways 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 older adults (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 a subset of 10 frontal and sensorimotor brain structures in the broader, distributed vestibular network: 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 Large Deformation Diffeomorphic Metric Mapping (LDDMM) surface registration. Shape descriptors were linearly regressed onto standardized vestibular variables, age, intracranial volume, sex, and in follow-up analyses, multisensory function (hearing, vision, proprioception). We found that 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 end-organ function and the focal morphology in aging in areas of the frontal and sensorimotor cortices relevant to executive ability, motor planning, and self-motion perception. An improved understanding of these pathways could help in developing interventions to enhance the quality of life in aging and populations with cognitive impairment.