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The Influence of Auditory Attention on Rhythmic Speech Tracking: Implications for Studies of Unresponsive Patients

Language comprehension relies on integrating words into progressively more complex structures, like phrases and sentences. This hierarchical structure-building is reflected in rhythmic neural activity across multiple timescales in E/MEG in healthy, awake participants. However, recent studies have sh...

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Autores principales: Sokoliuk, Rodika, Degano, Giulio, Melloni, Lucia, Noppeney, Uta, Cruse, Damian
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8385206/
https://www.ncbi.nlm.nih.gov/pubmed/34456697
http://dx.doi.org/10.3389/fnhum.2021.702768
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author Sokoliuk, Rodika
Degano, Giulio
Melloni, Lucia
Noppeney, Uta
Cruse, Damian
author_facet Sokoliuk, Rodika
Degano, Giulio
Melloni, Lucia
Noppeney, Uta
Cruse, Damian
author_sort Sokoliuk, Rodika
collection PubMed
description Language comprehension relies on integrating words into progressively more complex structures, like phrases and sentences. This hierarchical structure-building is reflected in rhythmic neural activity across multiple timescales in E/MEG in healthy, awake participants. However, recent studies have shown evidence for this “cortical tracking” of higher-level linguistic structures also in a proportion of unresponsive patients. What does this tell us about these patients’ residual levels of cognition and consciousness? Must the listener direct their attention toward higher level speech structures to exhibit cortical tracking, and would selective attention across levels of the hierarchy influence the expression of these rhythms? We investigated these questions in an EEG study of 72 healthy human volunteers listening to streams of monosyllabic isochronous English words that were either unrelated (scrambled condition) or composed of four-word-sequences building meaningful sentences (sentential condition). Importantly, there were no physical cues between four-word-sentences. Rather, boundaries were marked by syntactic structure and thematic role assignment. Participants were divided into three attention groups: from passive listening (passive group) to attending to individual words (word group) or sentences (sentence group). The passive and word groups were initially naïve to the sentential stimulus structure, while the sentence group was not. We found significant tracking at word- and sentence rate across all three groups, with sentence tracking linked to left middle temporal gyrus and right superior temporal gyrus. Goal-directed attention to words did not enhance word-rate-tracking, suggesting that word tracking here reflects largely automatic mechanisms, as was shown for tracking at the syllable-rate before. Importantly, goal-directed attention to sentences relative to words significantly increased sentence-rate-tracking over left inferior frontal gyrus. This attentional modulation of rhythmic EEG activity at the sentential rate highlights the role of attention in integrating individual words into complex linguistic structures. Nevertheless, given the presence of high-level cortical tracking under conditions of lower attentional effort, our findings underline the suitability of the paradigm in its clinical application in patients after brain injury. The neural dissociation between passive tracking of sentences and directed attention to sentences provides a potential means to further characterise the cognitive state of each unresponsive patient.
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spelling pubmed-83852062021-08-26 The Influence of Auditory Attention on Rhythmic Speech Tracking: Implications for Studies of Unresponsive Patients Sokoliuk, Rodika Degano, Giulio Melloni, Lucia Noppeney, Uta Cruse, Damian Front Hum Neurosci Neuroscience Language comprehension relies on integrating words into progressively more complex structures, like phrases and sentences. This hierarchical structure-building is reflected in rhythmic neural activity across multiple timescales in E/MEG in healthy, awake participants. However, recent studies have shown evidence for this “cortical tracking” of higher-level linguistic structures also in a proportion of unresponsive patients. What does this tell us about these patients’ residual levels of cognition and consciousness? Must the listener direct their attention toward higher level speech structures to exhibit cortical tracking, and would selective attention across levels of the hierarchy influence the expression of these rhythms? We investigated these questions in an EEG study of 72 healthy human volunteers listening to streams of monosyllabic isochronous English words that were either unrelated (scrambled condition) or composed of four-word-sequences building meaningful sentences (sentential condition). Importantly, there were no physical cues between four-word-sentences. Rather, boundaries were marked by syntactic structure and thematic role assignment. Participants were divided into three attention groups: from passive listening (passive group) to attending to individual words (word group) or sentences (sentence group). The passive and word groups were initially naïve to the sentential stimulus structure, while the sentence group was not. We found significant tracking at word- and sentence rate across all three groups, with sentence tracking linked to left middle temporal gyrus and right superior temporal gyrus. Goal-directed attention to words did not enhance word-rate-tracking, suggesting that word tracking here reflects largely automatic mechanisms, as was shown for tracking at the syllable-rate before. Importantly, goal-directed attention to sentences relative to words significantly increased sentence-rate-tracking over left inferior frontal gyrus. This attentional modulation of rhythmic EEG activity at the sentential rate highlights the role of attention in integrating individual words into complex linguistic structures. Nevertheless, given the presence of high-level cortical tracking under conditions of lower attentional effort, our findings underline the suitability of the paradigm in its clinical application in patients after brain injury. The neural dissociation between passive tracking of sentences and directed attention to sentences provides a potential means to further characterise the cognitive state of each unresponsive patient. Frontiers Media S.A. 2021-08-11 /pmc/articles/PMC8385206/ /pubmed/34456697 http://dx.doi.org/10.3389/fnhum.2021.702768 Text en Copyright © 2021 Sokoliuk, Degano, Melloni, Noppeney and Cruse. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Sokoliuk, Rodika
Degano, Giulio
Melloni, Lucia
Noppeney, Uta
Cruse, Damian
The Influence of Auditory Attention on Rhythmic Speech Tracking: Implications for Studies of Unresponsive Patients
title The Influence of Auditory Attention on Rhythmic Speech Tracking: Implications for Studies of Unresponsive Patients
title_full The Influence of Auditory Attention on Rhythmic Speech Tracking: Implications for Studies of Unresponsive Patients
title_fullStr The Influence of Auditory Attention on Rhythmic Speech Tracking: Implications for Studies of Unresponsive Patients
title_full_unstemmed The Influence of Auditory Attention on Rhythmic Speech Tracking: Implications for Studies of Unresponsive Patients
title_short The Influence of Auditory Attention on Rhythmic Speech Tracking: Implications for Studies of Unresponsive Patients
title_sort influence of auditory attention on rhythmic speech tracking: implications for studies of unresponsive patients
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8385206/
https://www.ncbi.nlm.nih.gov/pubmed/34456697
http://dx.doi.org/10.3389/fnhum.2021.702768
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