Electrophysiological markers of vestibular-mediated self-motion perception – A pilot study

[Display omitted] •A new cognitive vection paradigm was introduced without any visual, somatosensory, and auditory stimuli.•Alpha band EEG is linked to bottom-up vestibular sensory activation.•Theta band EEG is linked to self-motion perception per se.•Beta band EEG changes represent the process of u...

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Published inBrain research Vol. 1840; p. 149048
Main Authors Hadi, Zaeem, Pondeca, Yuscah, Rust, Heiko M., Seemungal, Barry M.
Format Journal Article
LanguageEnglish
Published Netherlands Elsevier B.V 01.10.2024
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Abstract [Display omitted] •A new cognitive vection paradigm was introduced without any visual, somatosensory, and auditory stimuli.•Alpha band EEG is linked to bottom-up vestibular sensory activation.•Theta band EEG is linked to self-motion perception per se.•Beta band EEG changes represent the process of updating of the prior brain state. Peripheral vestibular activation results in multi-level responses, from brainstem-mediated reflexes (e.g. vestibular ocular reflex – VOR) to perception of self-motion. While VOR responses indicate preserved vestibular peripheral and brainstem functioning, there are no automated measures of vestibular perception of self-motion – important since some patients with brain disconnection syndromes manifest a vestibular agnosia (intact VOR but impaired self-motion perception). Electroencephalography (‘EEG’) – may provide a surrogate marker of vestibular perception of self-motion. A related objective is obtaining an EEG marker of vestibular sensory signal processing, distinct from vestibular-motion perception. We performed a pilot study comparing EEG responses in the dark when healthy participants sat in a vibrationless computer-controlled motorised rotating chair moving at near threshold of self-motion perception, versus a second situation in which subjects sat in the chair at rest in the dark who could be induced (or not) into falsely perceiving self-motion. In both conditions subjects could perceive self-motion perception, but in the second there was no bottom-up reflex-brainstem activation. Time-frequency analyses showed: (i) alpha frequency band activity is linked to vestibular sensory-signal activation; and (ii) theta band activity is a marker of vestibular-mediated self-motion perception. Consistent with emerging animal data, our findings support the role of theta activity in the processing of self-motion perception.
AbstractList Graphical abstract
Peripheral vestibular activation results in multi-level responses, from brainstem-mediated reflexes (e.g. vestibular ocular reflex - VOR) to perception of self-motion. While VOR responses indicate preserved vestibular peripheral and brainstem functioning, there are no automated measures of vestibular perception of self-motion - important since some patients with brain disconnection syndromes manifest a vestibular agnosia (intact VOR but impaired self-motion perception). Electroencephalography ('EEG') - may provide a surrogate marker of vestibular perception of self-motion. A related objective is obtaining an EEG marker of vestibular sensory signal processing, distinct from vestibular-motion perception. We performed a pilot study comparing EEG responses in the dark when healthy participants sat in a vibrationless computer-controlled motorised rotating chair moving at near threshold of self-motion perception, versus a second situation in which subjects sat in the chair at rest in the dark who could be induced (or not) into falsely perceiving self-motion. In both conditions subjects could perceive self-motion perception, but in the second there was no bottom-up reflex-brainstem activation. Time-frequency analyses showed: (i) alpha frequency band activity is linked to vestibular sensory-signal activation; and (ii) theta band activity is a marker of vestibular-mediated self-motion perception. Consistent with emerging animal data, our findings support the role of theta activity in the processing of self-motion perception.Peripheral vestibular activation results in multi-level responses, from brainstem-mediated reflexes (e.g. vestibular ocular reflex - VOR) to perception of self-motion. While VOR responses indicate preserved vestibular peripheral and brainstem functioning, there are no automated measures of vestibular perception of self-motion - important since some patients with brain disconnection syndromes manifest a vestibular agnosia (intact VOR but impaired self-motion perception). Electroencephalography ('EEG') - may provide a surrogate marker of vestibular perception of self-motion. A related objective is obtaining an EEG marker of vestibular sensory signal processing, distinct from vestibular-motion perception. We performed a pilot study comparing EEG responses in the dark when healthy participants sat in a vibrationless computer-controlled motorised rotating chair moving at near threshold of self-motion perception, versus a second situation in which subjects sat in the chair at rest in the dark who could be induced (or not) into falsely perceiving self-motion. In both conditions subjects could perceive self-motion perception, but in the second there was no bottom-up reflex-brainstem activation. Time-frequency analyses showed: (i) alpha frequency band activity is linked to vestibular sensory-signal activation; and (ii) theta band activity is a marker of vestibular-mediated self-motion perception. Consistent with emerging animal data, our findings support the role of theta activity in the processing of self-motion perception.
[Display omitted] •A new cognitive vection paradigm was introduced without any visual, somatosensory, and auditory stimuli.•Alpha band EEG is linked to bottom-up vestibular sensory activation.•Theta band EEG is linked to self-motion perception per se.•Beta band EEG changes represent the process of updating of the prior brain state. Peripheral vestibular activation results in multi-level responses, from brainstem-mediated reflexes (e.g. vestibular ocular reflex – VOR) to perception of self-motion. While VOR responses indicate preserved vestibular peripheral and brainstem functioning, there are no automated measures of vestibular perception of self-motion – important since some patients with brain disconnection syndromes manifest a vestibular agnosia (intact VOR but impaired self-motion perception). Electroencephalography (‘EEG’) – may provide a surrogate marker of vestibular perception of self-motion. A related objective is obtaining an EEG marker of vestibular sensory signal processing, distinct from vestibular-motion perception. We performed a pilot study comparing EEG responses in the dark when healthy participants sat in a vibrationless computer-controlled motorised rotating chair moving at near threshold of self-motion perception, versus a second situation in which subjects sat in the chair at rest in the dark who could be induced (or not) into falsely perceiving self-motion. In both conditions subjects could perceive self-motion perception, but in the second there was no bottom-up reflex-brainstem activation. Time-frequency analyses showed: (i) alpha frequency band activity is linked to vestibular sensory-signal activation; and (ii) theta band activity is a marker of vestibular-mediated self-motion perception. Consistent with emerging animal data, our findings support the role of theta activity in the processing of self-motion perception.
Peripheral vestibular activation results in multi-level responses, from brainstem-mediated reflexes (e.g. vestibular ocular reflex - VOR) to perception of self-motion. While VOR responses indicate preserved vestibular peripheral and brainstem functioning, there are no automated measures of vestibular perception of self-motion - important since some patients with brain disconnection syndromes manifest a vestibular agnosia (intact VOR but impaired self-motion perception). Electroencephalography ('EEG') - may provide a surrogate marker of vestibular perception of self-motion. A related objective is obtaining an EEG marker of vestibular sensory signal processing, distinct from vestibular-motion perception. We performed a pilot study comparing EEG responses in the dark when healthy participants sat in a vibrationless computer-controlled motorised rotating chair moving at near threshold of self-motion perception, versus a second situation in which subjects sat in the chair at rest in the dark who could be induced (or not) into falsely perceiving self-motion. In both conditions subjects could perceive self-motion perception, but in the second there was no bottom-up reflex-brainstem activation. Time-frequency analyses showed: (i) alpha frequency band activity is linked to vestibular sensory-signal activation; and (ii) theta band activity is a marker of vestibular-mediated self-motion perception. Consistent with emerging animal data, our findings support the role of theta activity in the processing of self-motion perception.
ArticleNumber 149048
Author Hadi, Zaeem
Pondeca, Yuscah
Seemungal, Barry M.
Rust, Heiko M.
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Keywords Self-motion perception
Vestibular perception
Vection
Cognition
Illusory-self motion
EEG
Language English
License This is an open access article under the CC BY license.
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Snippet [Display omitted] •A new cognitive vection paradigm was introduced without any visual, somatosensory, and auditory stimuli.•Alpha band EEG is linked to...
Graphical abstract
Peripheral vestibular activation results in multi-level responses, from brainstem-mediated reflexes (e.g. vestibular ocular reflex - VOR) to perception of...
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StartPage 149048
SubjectTerms Cognition
EEG
Illusory-self motion
Neurology
Self-motion perception
Vection
Vestibular perception
Title Electrophysiological markers of vestibular-mediated self-motion perception – A pilot study
URI https://www.clinicalkey.com/#!/content/1-s2.0-S0006899324003020
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https://dx.doi.org/10.1016/j.brainres.2024.149048
https://www.ncbi.nlm.nih.gov/pubmed/38844198
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