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

  • 1Sleep and Epilepsy Unit, IRCCS Mondino Foundation, Pavia, Italy; Department of Brain and Behavioural Sciences, University of Pavia, Pavia, Italy.
  • 2Claudio Munari" Centre for Epilepsy Surgery, ASST GOM Niguarda, Milan, Italy; Department of Medicine and Surgery, Unit of Neuroscience, University of Parma, Parma, Italy. Electronic address: piergiorgio.dorio@ospedaleniguarda.it.
  • 3Claudio Munari" Centre for Epilepsy Surgery, ASST GOM Niguarda, Milan, Italy.
  • 4Claudio Munari" Centre for Epilepsy Surgery, ASST GOM Niguarda, Milan, Italy; Department of Philosophy "Piero Martinetti", University of Milan, Milan, Italy; Department of Biomedical and Clinical Sciences "L. Sacco", University of Milan, Milan, Italy.
  • 5SC Neurology and Stroke Unit, Ospedale Civile di Voghera, Dipartimento interaziendale di Neuroscienze, ASST Pavia, Italy.
  • 6Department of Brain and Behavioural Sciences, University of Pavia, Pavia, Italy.
  • 7Istituto di Neuroscienze, Consiglio Nazionale delle Ricerche, Parma, Italy.
  • 8Istituto Clinico Mater Domini Humanitas, Castellanza, Italy; Istituto Auxologico Capitanio, IRCCS, Milan, Italy.

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Abstract

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.

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