Oscillatory neural responses evoked by natural vestibular stimuli in humans

Abstract

While there have been numerous studies of the vestibular system in mammals, less is known about the brain mechanisms of vestibular processing in humans. In particular, of the studies that have been carried out in humans over the last 30 years, none has investigated how vestibular stimulation (VS) affects cortical oscillations. Here we recorded high-density electroencephalography (EEG) in healthy human subjects and a group of bilateral vestibular loss patients (BVPs) undergoing transient and constant-velocity passive whole body yaw rotations, focusing our analyses on the modulation of cortical oscillations in response to natural VS. The present approach overcame significant technical challenges associated with combining natural VS with human electrophysiology and reveals that both transient and constant-velocity VS are associated with a prominent suppression of alpha power (8 -13 Hz). Alpha band suppression was localized over bilateral temporo-parietal scalp regions, and these alpha modulations were significantly smaller in BVPs. We propose that suppression of oscillations in the alpha band over temporo-parietal scalp regions reflects cortical vestibular processing, potentially comparable with alpha and mu oscillations in the visual and sensorimotor systems, respectively, opening the door to the investigation of human cortical processing under various experimental conditions during natural VS. EEG; vestibular processing; vestibular cortex THE VESTIBULAR SYSTEM encodes three-dimensional displacements of the head and its position relative to gravity. Vestibular signals are used for oculomotor and postural control but also underpin perceptual and cognitive functions, including visual perception according to internal models of gravity, spatial navigation, and bodily awareness (Brandt et al. 2005;Indovina et al. 2005;Lopez et al. 2010). In strong contrast with the growing number of functions shown to be under vestibular influence is the relative lack of data on the vestibular cortex in animals and humans (Angelaki and Cullen 2008;Brandt and Dieterich 1999;Lopez and Blanke 2011).Electrophysiological investigations in nonhuman primates have revealed vestibular responses in several areas of the cortex. These include the intraparietal sulcus and the somatosensory, temporal, frontal, and parieto-insular cortices (Bremmer et al. 2002;Grüsser et al. 1990aGrüsser et al. , 1990bGu et al. 2008;Liu et al. 2011;Schwarz and Fredrickson 1971). These areas form a cortical network of which the core is presumed to be located in the "parieto-insular vestibular cortex" (PIVC; Guldin and Grüsser 1998). Recently, descriptions of vestibular neurons' spatiotemporal tuning in these cortical regions have been achieved during three-dimensional passive rotations/ translations on motion platforms in nonhuman primates (e.g., Chen et al. 2011;Shinder and Newlands 2014;Takahashi et al. 2007).Investigations of the human vestibular cortex are challenging because neuroimaging techniques (fMRI, PET) do not allow head and body movements and thus the app...

Vestibular contributions to high-level sensorimotor functions

“…This overall reduction in alpha band power reflects self-motion processing irrespective of the target updating. A similar suppression of alpha band activity in parietal areas has recently been reported for rotational self-motion (Gale et al, 2015).…”

Positron emission tomography visualized stimulation of the vestibular organ is localized in Heschl's gyrus

“…No response to otolith stimulation was found in this PIVC area, and the neighboring area designated as purely auditory was not investigated for electrophysiological responses during vestibular stimulation (Guldin, Akbarian, & Grusser, ). It is also important to acknowledge that data from non‐human primates during natural vestibular stimulation on motion platforms might differ from human data during artificial vestibular stimulation (Gale et al, ).…”

Vestibular modulation of peripersonal space boundaries

“…Participants passively received whole‐body yaw rotations in clockwise (Rightward Rotation) or counterclockwise (Leftward Rotation) direction about a head‐centered earth‐vertical axis. This experimental setup has been used previously in several studies (Prsa et al ., ; van Elk & Blanke, ; Ferrè et al ., ; Gale et al ., ; Kaliuzhna et al ., ; Pfeiffer et al ., ). At the beginning of an experimental trial, the platform accelerated in clockwise or counterclockwise direction from 0 °/s to 140 °/s maximum velocity following a cosine‐smoothed acceleration profile (i.e., Gaussian shape, 70 °/s 2 maximum acceleration reached at 2 s after onset) during 4 s. This acceleration profile was chosen because the semicircular canals are maximally tuned to such cosine‐smoothed accelerations resembling natural voluntary head movements (Bertolini et al ., ; Prsa et al ., ).…”