Age-dependent vestibular cingulate–cerebral network underlying gravitational perception: a cross-sectional multimodal study

Abstract

Background and objectives

The cingulate gyrus (CG) is a frequently studied yet not wholly understood area of the human cerebrum. Previous studies have implicated CG in different adaptive cognitive–emotional functions and fascinating or debilitating symptoms. We describe an unusual loss of gravity perception/floating sensation in consecutive persons with drug-resistant epilepsy undergoing electrical cortical stimulation (ECS), network analysis, and network robustness mapping.

Methods

Using Intracranial–EEG, Granger causality analysis, cortico-cortical evoked potentials, and fMRI, we explicate the functional networks arising from this phenomenon's anterior, middle, and posterior cingulate cortex.

Results

Fifty-four icEEG cases from 2013 to 2019 were screened. In 40.7% of cases, CG was sampled and in 22.2% the sampling was bilateral. ECS mapping was carried out in 18.5% of the entire cohort and 45.4% of the cingulate sampled cases. Five of the ten CG cases experienced symptoms during stimulation. A total of 1942 electrodes were implanted with a median number of 182 electrode contacts per patient (range: 106–274). The electrode contacts sampled all major cortex regions. Sixty-three contacts were within CG. Of those, 26 were electrically stimulated; 53.8% of the stimulated contacts produced positive responses, whereas 46.2% produced no observable responses. Our study reports a unique perceptive phenomenon of a subjective sense of weightlessness/floating sensation triggered by anterior and posterior CG stimulation, in 30% of cases and 21.42% of electrode stimulation sites. Notable findings include functional connections between the insula, the posterior and anterior cingulate cortex, and networks between the middle cingulate and the frontal and temporal lobes and the cerebellum. We also postulate a vestibular–cerebral–cingulate network responsible for the perception of gravity while suggesting that cingulate functional connectivity follows a long-term developmental trajectory as indicated by a robust, positive correlation with age and the extent of Granger connectivity (r = 0.82, p = 0.0035).

Discussion

We propose, in conjunction with ECS techniques, that a better understanding of the underlying gravity perception networks can lead to promising neuromodulatory clinical applications.

Classification of evidence

This study provides Class II evidence for CG's involvement in the higher order processing of gravity perception and related actions.