Journal Article

Spatio-temporal dynamics of sound-induced vestibular processing: insights from stereo-EEG recordings

Colnaghi, Silvia, Rustioni, Valter, Versino, Maurizio, Pelliccia, Veronica, Terzaghi, Michele, d'Orio, Piergiorgio, Zauli, Flavia Maria, Caruana, Fausto, Vecchio, Maria Del, Avanzini, Pietro, Sartori, Ivana

2025

Overview

•Vestibular system processes sensory inputs key to posture, gaze, and spatial memory.•Vestibular processing areas are well-mapped, but timing integration remains unclear.•Early vestibular processing involves parallel pathways, not a single primary cortex.•Dorsal and ventral streams aid vestibulo-motor integration and retention over time.•Vestibular system complexity links spatio-temporal dynamics to body awareness. Numerous functions rely on the activation of the vestibular system, resulting in widespread activation of cortical brain regions. However, although the topographical organization of vestibular processing is relatively well understood, the temporal dynamics of this information processing remain insufficiently explored. In this study, we conducted an in-depth analysis of intracerebral recordings from 107 patients (123 implanted hemispheres) to investigate the cortical response to acoustic and sound-induced vestibular stimuli (SVS), thus unveiling the spatiotemporal dynamics of vestibular processing. Our findings revealed the existence of distinct early components (phasic peak, 20–40 ms) localized in Heschl's area, planum temporale, retroinsula, posterior insular cortex, PFcm, parietal operculum, and structures above the Sylvian fissure. Moreover, we identified later, tonic components (peaking at 50–80 ms) characterized by an extended duration, returning to baseline between 200 and 300 ms. Remarkably, these latter components exclusively involved the perisylvian cortices. The findings demonstrated that the early stages of human otolithic vestibular information processing involve both parallel and hierarchical pathways distributed across the perisylvian and peri‑Rolandic regions, rather than being restricted to a single primary cortical area. Furthermore, two distinct streams reminiscent of the dorsal/ventral dichotomy with specific spatio-temporal characteristics were identified. Collectively, our study uncovers a complex and interconnected cortical network that underlies vestibular processing, shedding light on the temporal dynamics of this essential sensory system. These findings pave the way for a deeper understanding of the functional organization of the vestibular system and its implications for sensory perception and motor control. The vestibular system plays a crucial role in daily life by responding to various sensory inputs. We observed a complex and interconnected cortical network shedding light on its temporal dynamics. The results revealed that vestibular processing involves parallel and hierarchical pathways rather than a single primary cortex and a dorsal/ventral stream dichotomy was identified. [Display omitted]

• Publisher: Elsevier Inc,Elsevier Limited,Elsevier
• Subject: Acoustic Stimulation / Acoustics / Adult / Auditory Perception - physiology / Brain Mapping - methods / Cerebral Cortex - physiology / Convulsions & seizures / Cortex (insular) / Cortex (parietal) / Decomposition / Electrodes / Electroencephalography / Electroencephalography - methods / Epilepsy / Female / Four-dimensional maps / Functional morphology / Humans / Information processing / Localization / Male / Medical imaging / Middle Aged / Motor task performance / Neuroimaging / Operculum / Patients / Planum temporale / Radiology/Diagnostic Imaging / Somatosensory cortex / Stereo-EEG / Temporal lobe / Vestibular evoked myogenic potentials / Vestibular stimuli / Vestibular system / Vestibule, Labyrinth - physiology / Young Adult