Structural and functional connectivity of vestibular graviceptive to sensory and motor circuits.

Abstract

Processing of vestibular graviceptive signals from the inner ear is essential for spatial perception, bipedal stance, locomotion, and navigation in a three-dimensional world. Acute unilateral ischaemic lesions along the central vestibular pathways lead to deficits of gravitational processing which can be quantified as perceptual tilts of the subjective visual vertical (SVV). For ipsiversive and contraversive directional tilts, dichotomous networks were documented from the brainstem to the thalamus. In the current lesion-network mapping study, we asked whether this dichotomy of directional tilts of gravitational processing is maintained at the cortical level. 107 patients with acute right-hemispheric infarcts (mean age 66 years, ±13 years) in the territory of the middle cerebral artery were included in the study. To examine the association of tilts of the SVV with lesion locations, support-vector regression lesion-symptom mapping (SVR-LSM) was used with tilt of the SVV as a continuous variable. Analyses were carried out for ipsi- and contraversive tilts separately. In addition, we performed disconnectome mapping and SVR-LSM-disconnectome analyses by referencing lesions to a normative connectome detect structural networks associated with SVV tilts. Similarly, functional connectivity mapping was used to determine the functional networks associated with SVV tilts. The SVR-LSM with the functional maps revealed the statistical association between SVV tilt and functional networks. The SVR-LSM analysis demonstrated distinct clusters associated with either ipsi- or contraversive SVV tilts. Ipsiversive tilt clusters were centered around the parieto-(retro)-insular opercular cortex [PIVC, retroinsular area (Ri), posterior insular long gyrus (Ig), parietal operculum (OP2-3)]. The contraversive tilt cluster showed additional involvement of the motor system (basal ganglia) and the ventral prefrontal cortex (Brodman area BA44, inferior frontal gyrus). In lesions with ipsiversive tilts, a disconnection of fronto-insular tracts and the arcuate fascicle was found. Contraversive tilt related disconnection was observed in the superior longitudinal fascicle (SLFII) and the medial temporal cortex (perirhinal, entorhinal cortex). Cortico-fugal connections could be traced down via the thalamus to the cerebellum and vestibular nuclei. The functional networks associated with ipsiversive and contraversive tilts showed a similar pattern: more restricted in the core vestibular and ocular motor cortical network for ipsiversive tilts, additional involvement of the motor system for contraversive tilts. Thus, the current data demonstrate partly separated cortical networks for gravitational processing associated with directional SVV tilts. These could imply differential routes of vestibular input for sensory and motor processing.