Padova Dominic, Ratnanather J Tilak, Faria Andreia V, Agrawal Yuri
Center for Imaging Science, Department of Biomedical Engineering, Johns Hopkins University, Baltimore, Maryland, USA.
Center for Imaging Science and Institute for Computational Medicine, Department of Biomedical Engineering, Johns Hopkins University, Baltimore, Maryland, USA.
Hum Brain Mapp. 2025 Jul;46(10):e70251. doi: 10.1002/hbm.70251.
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.
外周前庭功能的衰老相关衰退与已知依赖于感觉运动和额叶皮质的行为及认知能力缺陷有关，但确切的神经通路尚不清楚。为填补这一知识空白，这项横断面研究考察了前庭功能的年龄相关变化与额叶和感觉运动皮质表面形状改变之间的关系，同时考虑了年龄、颅内体积和性别。分析了来自巴尔的摩老年纵向研究的117名老年人（60岁以上）的数据，这些老年人在同一次就诊时接受了终末器官特异性前庭测试（球囊的颈肌前庭诱发肌源性电位、椭圆囊的眼肌前庭诱发肌源性电位和水平半规管的视频头脉冲试验）以及T1加权磁共振成像扫描。我们在更广泛的分布式前庭网络中检查了10个额叶和感觉运动脑结构的子集：前额叶皮质的中上部分（额上回中上部）、额极、额上回后部、背侧前额叶皮质和额中回后部（额中回背侧后部、额中回）、额下回的岛盖部、三角部和眶部，以及感觉运动皮质的中央前回和中央后回。对于每个感兴趣区域（ROI），使用大变形微分同胚度量映射（LDDMM）表面配准将形状描述符估计为群体平均ROI表面的局部压缩和扩展。将形状描述符与标准化前庭变量、年龄、颅内体积、性别进行线性回归，并在后续分析中与多感官功能（听力、视力、本体感觉）进行线性回归。我们发现，椭圆囊功能降低与左侧额中回表面压缩以及双侧额极和左侧额上回表面扩张有关。半规管功能降低与右侧额上回中上部和额极以及左侧额上回表面压缩有关。球囊和椭圆囊功能降低均与左侧额中回后部内侧表面压缩相关。我们的研究结果揭示了前庭终末器官功能与额叶和感觉运动皮质中与执行能力、运动规划和自我运动感知相关区域衰老中的局灶形态之间关系的复杂性。对这些通路的更好理解有助于开发干预措施，以提高老年人和认知障碍人群的生活质量。
