Subclinical Vestibular Function is Associated with Surface Shape Changes in the Prefrontal Cortex

Poster No:

1201 

Submission Type:

Abstract Submission 

Authors:

Dominic Padova1, Andreia Faria1, Yuri Agrawal2, Tilak Ratnanather1

Institutions:

1Johns Hopkins University, Baltimore, MD, 2University of Colorado School of Medicine, Denver, CO

First Author:

Dominic Padova  
Johns Hopkins University
Baltimore, MD

Co-Author(s):

Andreia Faria  
Johns Hopkins University
Baltimore, MD
Yuri Agrawal  
University of Colorado School of Medicine
Denver, CO
Tilak Ratnanather  
Johns Hopkins University
Baltimore, MD

Introduction:

Aging-associated decline in peripheral vestibular function is linked to deficits in cognitive abilities like attention, executive function, and motor planning, highlighting the prefrontal cortex's significance. Functional neuroimaging suggests a vestibular-thalamus-prefrontal cortex pathway, with notable activations in the frontal gyri, but the exact neuroanatomical pathways remain unclear. Subclinical declines in vestibular function correlate with thalamic shape abnormalities, yet the specific involvement of prefrontal cortex subregions is not consistently demonstrated in structural neuroimaging of vestibular patients. To bridge this knowledge gap, this study investigates the relationship between subclinical vestibular function and surface shape changes in eight prefrontal cortex subfields, considering age, intracranial volume, and sex.

Methods:

Data from 117 participants aged 60+ from the Baltimore Longitudinal Study of Aging, who underwent concurrent end-organ-specific vestibular tests (cVEMP for the saccule, oVEMP for the utricle, and vHIT for the horizonal canal) and T1-weighted MRI scans, were analyzed. This data was used in a previous study of a different cognitive network. MRI scans were segmented automatically using MRICloud. Surface meshes were generated using a restricted Delaunay triangulation. Population templates were created independently for each hemisphere of every region of interest and mapped to individual surfaces to measure surface shape change (tangent, normal). To streamline statistical testing, the 800 surface vertices were clustered into k patches of ≈150 mm2 based on surface geometry, reducing the number of comparisons thirtyfold. Shape variables were linearly regressed on standardized vestibular variables and covariates. Hypotheses were tested using 10,000 permutations, with a FWER rejection threshold set at the 0.05 level based on the maximum test statistic across the surface. Quality control was performed at each stage.

Results:

No relationships between vestibular function and the shape of the superior frontal gyrus (SFG, SFG_PFC, SFG_pole) or the MFG_DPFC survived FWER correction at 0.05 level. A 1 standard deviation (SD) increase in saccular function was associated with ≈0.102% compression tangent to the cortical surface in Cluster 11 of the left pars opercularis (p≈0.027) and with ≈0.077% expansion normal to the cortical surface in Cluster 13 of the left middle frontal gyrus (p≈0.072). A 1 SD increase in utricular function correlated with ≈0.093% and ≈0.065% compressions tangent and normal to the cortical surface in Cluster 3 of the right pars orbitalis, respectively (p≈0.017 and p≈0.008). A 1 SD increase in horizontal semi-circular canal function correlated with ≈0.1% and ≈0.074% compression tangent and normal to the cortical surface in Cluster 4 of the left pars triangularis (p≈0.004 and p≈0.0001).

Conclusions:

We found associations between reduced saccular function and significant cortical surface compression in the middle frontal gyrus and expansion in the pars opercularis, and reduced utricular and canal functions and significant surface expansion in the pars orbitalis and pars triangularis of the inferior frontal gyrus, respectively. Our significant regions agree with some of those reported in several neuroimaging studies of healthy adults and vestibular patients, clarifying previous equivocal findings. Furthermore, these findings may provide the neuroanatomical links through which vestibular end-organ function impacts higher-order cognitive abilities in the aging population.

Lifespan Development:

Aging 1

Modeling and Analysis Methods:

Image Registration and Computational Anatomy 2
Univariate Modeling

Neuroanatomy, Physiology, Metabolism and Neurotransmission:

Cortical Anatomy and Brain Mapping

Novel Imaging Acquisition Methods:

Anatomical MRI

Keywords:

Aging
Cortex
STRUCTURAL MRI

1|2Indicates the priority used for review

Provide references using author date format

[1] Bigelow, R. T., & Agrawal, Y. (2015). Vestibular involvement in cognition: Visuospatial ability, attention, executive function, and memory. Journal of Vestibular Research, 25(2), 73-89.
[2] Lopez C, Blanke O. (2011). ‘The thalamocortical vestibular system in animals and humans’, Brain research reviews, vol. 67, no. 1-2, pp. 119-146.
[3] De Waele, C., Baudonnière, P., Lepecq, J., Tran Ba Huy, P., & Vidal, P. (2001). Vestibular projections in the human cortex. Experimental brain research, 141, 541-551.
[4] Miyamoto, T., Fukushima, K., Takada, T., de Waele, C., & Vidal, P. P. (2007). Saccular stimulation of the human cortex: a functional magnetic resonance imaging study. Neuroscience letters, 423(1), 68-72.
[5] Jacob A, Tward DJ, Resnick S, Smith PF, Lopez C, Rebello E, Wei EX, Ratnanather JT, Agrawal Y. (2020). ‘Vestibular function and cortical and sub-cortical alterations in an aging population’, Heliyon, vol. 6, no. 8, pp. e04728.
[6] Hong, S. K., Kim, J. H., Kim, H. J., & Lee, H. J. (2014). Changes in the gray matter volume during compensation after vestibular neuritis: a longitudinal VBM study. Restorative Neurology and Neuroscience, 32(5), 663-673.
[7] Hufner K, Stephan T, Hamilton D, Kalla R, Glasauer S, Strupp M, Brandt T. (2009). ‘Gray-matter atrophy after chronic complete unilateral vestibular deafferentation’, Annals of the New York Academy of Sciences, vol. 1164, no. 1, pp. 383-5.
[8] zu Eulenburg P, Stoeter P, Dieterich M. (2010). ‘Voxel‐based morphometry depicts central compensation after vestibular neuritis’, Annals of neurology, vol. 68, no. 2, pp. 241-9.
[9] Wurthmann S, Naegel S, Steinberg BS, Theysohn N, Diener HC, Kleinschnitz C, Obermann M, Holle D. (2017). ‘Cerebral gray matter changes in persistent postural perceptual dizziness’, Journal of psychosomatic research, vol. 103, pp. 95-101.