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Unexpected sound omissions are signaled in human posterior superior temporal gyrus: an intracranial study.

ABSTRACT: Context modulates sensory neural activations enhancing perceptual and behavioral performance and reducing prediction errors. However, the mechanism of when and where these high-level expectations act on sensory processing is unclear. Here, we isolate the effect of expectation absent of any auditory evoked activity by assessing the response to omitted expected sounds. Electrocorticographic signals were recorded directly from subdural electrode grids placed over the superior temporal gyrus (STG). Subjects listened to a predictable sequence of syllables, with some infrequently omitted. We found high-frequency band activity (HFA, 70-170 Hz) in response to omissions, which overlapped with a posterior subset of auditory-active electrodes in STG. Heard syllables could be distinguishable reliably from STG, but not the identity of the omitted stimulus. Both omission- and target-detection responses were also observed in the prefrontal cortex. We propose that the posterior STG is central for implementing predictions in the auditory environment. HFA omission responses in this region appear to index mismatch-signaling or salience detection processes.

SUBMITTER: Cho H

PROVIDER: S-EPMC10350817 | biostudies-literature | 2023 Jul

REPOSITORIES: biostudies-literature

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Unexpected sound omissions are signaled in human posterior superior temporal gyrus: an intracranial study.

Cho Hohyun H Fonken Yvonne M YM Adamek Markus M Jimenez Richard R Lin Jack J JJ Schalk Gerwin G Knight Robert T RT Brunner Peter P

Cerebral cortex (New York, N.Y. : 1991) 20230701 14

Context modulates sensory neural activations enhancing perceptual and behavioral performance and reducing prediction errors. However, the mechanism of when and where these high-level expectations act on sensory processing is unclear. Here, we isolate the effect of expectation absent of any auditory evoked activity by assessing the response to omitted expected sounds. Electrocorticographic signals were recorded directly from subdural electrode grids placed over the superior temporal gyrus (STG). ...[more]

PMID: 37280730

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Project description:Experimentalists studying multisensory integration compare neural responses to multisensory stimuli with responses to the component modalities presented in isolation. This procedure is problematic for multisensory speech perception since audiovisual speech and auditory-only speech are easily intelligible but visual-only speech is not. To overcome this confound, we developed intracranial encephalography (iEEG) deconvolution. Individual stimuli always contained both auditory and visual speech, but jittering the onset asynchrony between modalities allowed for the time course of the unisensory responses and the interaction between them to be independently estimated. We applied this procedure to electrodes implanted in human epilepsy patients (both male and female) over the posterior superior temporal gyrus (pSTG), a brain area known to be important for speech perception. iEEG deconvolution revealed sustained positive responses to visual-only speech and larger, phasic responses to auditory-only speech. Confirming results from scalp EEG, responses to audiovisual speech were weaker than responses to auditory-only speech, demonstrating a subadditive multisensory neural computation. Leveraging the spatial resolution of iEEG, we extended these results to show that subadditivity is most pronounced in more posterior aspects of the pSTG. Across electrodes, subadditivity correlated with visual responsiveness, supporting a model in which visual speech enhances the efficiency of auditory speech processing in pSTG. The ability to separate neural processes may make iEEG deconvolution useful for studying a variety of complex cognitive and perceptual tasks.SIGNIFICANCE STATEMENT Understanding speech is one of the most important human abilities. Speech perception uses information from both the auditory and visual modalities. It has been difficult to study neural responses to visual speech because visual-only speech is difficult or impossible to comprehend, unlike auditory-only and audiovisual speech. We used intracranial encephalography deconvolution to overcome this obstacle. We found that visual speech evokes a positive response in the human posterior superior temporal gyrus, enhancing the efficiency of auditory speech processing.

Dataset Information

Unexpected sound omissions are signaled in human posterior superior temporal gyrus: an intracranial study.

Publications

Unexpected sound omissions are signaled in human posterior superior temporal gyrus: an intracranial study.

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