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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Main Authors: Rodika Sokoliuk, Giulio Degano, Lucia Melloni, Uta Noppeney, Damian Cruse
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-08-01
Series:Frontiers in Human Neuroscience
Subjects:
EEG
Online Access:https://www.frontiersin.org/articles/10.3389/fnhum.2021.702768/full
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spelling doaj-d556a7545c694aecbc6596bd0590ecff2021-08-11T05:11:43ZengFrontiers Media S.A.Frontiers in Human Neuroscience1662-51612021-08-011510.3389/fnhum.2021.702768702768The Influence of Auditory Attention on Rhythmic Speech Tracking: Implications for Studies of Unresponsive PatientsRodika Sokoliuk0Rodika Sokoliuk1Giulio Degano2Giulio Degano3Giulio Degano4Lucia Melloni5Lucia Melloni6Uta Noppeney7Uta Noppeney8Damian Cruse9Damian Cruse10School of Psychology, University of Birmingham, Birmingham, United KingdomCentre for Human Brain Health, University of Birmingham, Birmingham, United KingdomSchool of Psychology, University of Birmingham, Birmingham, United KingdomCentre for Human Brain Health, University of Birmingham, Birmingham, United KingdomBrain and Language Lab, Department of Psychology, Faculty of Psychology and Educational Sciences, University of Geneva, Geneva, SwitzerlandMax Planck Institute for Empirical Aesthetics, Frankfurt, GermanyDepartment of Neurology, New York University, New York City, NY, United StatesDonders Centre for Cognitive Neuroimaging, Nijmegen, NetherlandsDepartment of Biophysics, Radboud University, Nijmegen, NetherlandsSchool of Psychology, University of Birmingham, Birmingham, United KingdomCentre for Human Brain Health, University of Birmingham, Birmingham, United KingdomLanguage 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.https://www.frontiersin.org/articles/10.3389/fnhum.2021.702768/fullcortical trackingbrain oscillationsEEGattentionspeech trackingunresponsive patients
collection DOAJ
language English
format Article
sources DOAJ
author Rodika Sokoliuk
Rodika Sokoliuk
Giulio Degano
Giulio Degano
Giulio Degano
Lucia Melloni
Lucia Melloni
Uta Noppeney
Uta Noppeney
Damian Cruse
Damian Cruse
spellingShingle Rodika Sokoliuk
Rodika Sokoliuk
Giulio Degano
Giulio Degano
Giulio Degano
Lucia Melloni
Lucia Melloni
Uta Noppeney
Uta Noppeney
Damian Cruse
Damian Cruse
The Influence of Auditory Attention on Rhythmic Speech Tracking: Implications for Studies of Unresponsive Patients
Frontiers in Human Neuroscience
cortical tracking
brain oscillations
EEG
attention
speech tracking
unresponsive patients
author_facet Rodika Sokoliuk
Rodika Sokoliuk
Giulio Degano
Giulio Degano
Giulio Degano
Lucia Melloni
Lucia Melloni
Uta Noppeney
Uta Noppeney
Damian Cruse
Damian Cruse
author_sort Rodika Sokoliuk
title 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_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_sort influence of auditory attention on rhythmic speech tracking: implications for studies of unresponsive patients
publisher Frontiers Media S.A.
series Frontiers in Human Neuroscience
issn 1662-5161
publishDate 2021-08-01
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.
topic cortical tracking
brain oscillations
EEG
attention
speech tracking
unresponsive patients
url https://www.frontiersin.org/articles/10.3389/fnhum.2021.702768/full
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