Spontaneous Neural Activity in the Superior Temporal Gyrus Recapitulates Tuning for Speech Features

Background: Numerous studies have demonstrated that individuals exhibit structured neural activity in many brain regions during rest that is also observed during different tasks, however it is still not clear whether and how resting state activity patterns may relate to underlying tuning for specifi...

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Main Authors: Jonathan D. Breshears, Liberty S. Hamilton, Edward F. Chang
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-09-01
Series:Frontiers in Human Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fnhum.2018.00360/full
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author Jonathan D. Breshears
Liberty S. Hamilton
Liberty S. Hamilton
Liberty S. Hamilton
Edward F. Chang
author_facet Jonathan D. Breshears
Liberty S. Hamilton
Liberty S. Hamilton
Liberty S. Hamilton
Edward F. Chang
author_sort Jonathan D. Breshears
collection DOAJ
description Background: Numerous studies have demonstrated that individuals exhibit structured neural activity in many brain regions during rest that is also observed during different tasks, however it is still not clear whether and how resting state activity patterns may relate to underlying tuning for specific stimuli. In the posterior superior temporal gyrus (STG), distinct neural activity patterns are observed during the perception of specific linguistic speech features. We hypothesized that spontaneous resting-state neural dynamics of the STG would be structured to reflect its role in speech perception, exhibiting an organization along speech features as seen during speech perception.Methods: Human cortical local field potentials were recorded from the superior temporal gyrus (STG) in 8 patients undergoing surgical treatment of epilepsy. Signals were recorded during speech perception and rest. Patterns of neural activity (high gamma power: 70–150 Hz) during rest, extracted with spatiotemporal principal component analysis, were compared to spatiotemporal neural responses to speech features during perception. Hierarchical clustering was applied to look for patterns in rest that corresponded to speech feature tuning.Results: Significant correlations were found between neural responses to speech features (sentence onsets, consonants, and vowels) and the spontaneous neural activity in the STG. Across subjects, these correlations clustered into five groups, demonstrating tuning for speech features—most robustly for acoustic onsets. These correlations were not seen in other brain areas, or during motor and spectrally-rotated speech control tasks.Conclusions: In this study, we present evidence that the RS structure of STG activity robustly recapitulates its stimulus-evoked response to acoustic onsets. Further, secondary patterns in RS activity appear to correlate with stimulus-evoked responses to speech features. The role of these spontaneous spatiotemporal activity patterns remains to be elucidated.
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spelling doaj.art-5c0fa1f8cc9243ae90588ff86fec011e2022-12-21T17:49:19ZengFrontiers Media S.A.Frontiers in Human Neuroscience1662-51612018-09-011210.3389/fnhum.2018.00360404350Spontaneous Neural Activity in the Superior Temporal Gyrus Recapitulates Tuning for Speech FeaturesJonathan D. Breshears0Liberty S. Hamilton1Liberty S. Hamilton2Liberty S. Hamilton3Edward F. Chang4Department of Neurosurgery, University of California, San Francisco, San Francisco, CA, United StatesDepartment of Neurosurgery, University of California, San Francisco, San Francisco, CA, United StatesDepartment of Communication Sciences and Disorders, University of Texas at Austin, Austin, TX, United StatesDepartment of Neurology, Dell Medical School, University of Texas at Austin, Austin, TX, United StatesDepartment of Neurosurgery, University of California, San Francisco, San Francisco, CA, United StatesBackground: Numerous studies have demonstrated that individuals exhibit structured neural activity in many brain regions during rest that is also observed during different tasks, however it is still not clear whether and how resting state activity patterns may relate to underlying tuning for specific stimuli. In the posterior superior temporal gyrus (STG), distinct neural activity patterns are observed during the perception of specific linguistic speech features. We hypothesized that spontaneous resting-state neural dynamics of the STG would be structured to reflect its role in speech perception, exhibiting an organization along speech features as seen during speech perception.Methods: Human cortical local field potentials were recorded from the superior temporal gyrus (STG) in 8 patients undergoing surgical treatment of epilepsy. Signals were recorded during speech perception and rest. Patterns of neural activity (high gamma power: 70–150 Hz) during rest, extracted with spatiotemporal principal component analysis, were compared to spatiotemporal neural responses to speech features during perception. Hierarchical clustering was applied to look for patterns in rest that corresponded to speech feature tuning.Results: Significant correlations were found between neural responses to speech features (sentence onsets, consonants, and vowels) and the spontaneous neural activity in the STG. Across subjects, these correlations clustered into five groups, demonstrating tuning for speech features—most robustly for acoustic onsets. These correlations were not seen in other brain areas, or during motor and spectrally-rotated speech control tasks.Conclusions: In this study, we present evidence that the RS structure of STG activity robustly recapitulates its stimulus-evoked response to acoustic onsets. Further, secondary patterns in RS activity appear to correlate with stimulus-evoked responses to speech features. The role of these spontaneous spatiotemporal activity patterns remains to be elucidated.https://www.frontiersin.org/article/10.3389/fnhum.2018.00360/fullelectrocorticography (ECoG)speech perceptionhigh gamma activityresting state networksspatiotemporal dynamics
spellingShingle Jonathan D. Breshears
Liberty S. Hamilton
Liberty S. Hamilton
Liberty S. Hamilton
Edward F. Chang
Spontaneous Neural Activity in the Superior Temporal Gyrus Recapitulates Tuning for Speech Features
Frontiers in Human Neuroscience
electrocorticography (ECoG)
speech perception
high gamma activity
resting state networks
spatiotemporal dynamics
title Spontaneous Neural Activity in the Superior Temporal Gyrus Recapitulates Tuning for Speech Features
title_full Spontaneous Neural Activity in the Superior Temporal Gyrus Recapitulates Tuning for Speech Features
title_fullStr Spontaneous Neural Activity in the Superior Temporal Gyrus Recapitulates Tuning for Speech Features
title_full_unstemmed Spontaneous Neural Activity in the Superior Temporal Gyrus Recapitulates Tuning for Speech Features
title_short Spontaneous Neural Activity in the Superior Temporal Gyrus Recapitulates Tuning for Speech Features
title_sort spontaneous neural activity in the superior temporal gyrus recapitulates tuning for speech features
topic electrocorticography (ECoG)
speech perception
high gamma activity
resting state networks
spatiotemporal dynamics
url https://www.frontiersin.org/article/10.3389/fnhum.2018.00360/full
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