Neural Mechanisms Underlying the Effects of Novel Sounds on Task Performance in Children With and Without ADHD

Distractibility is one of the key features of attention deficit hyperactivity disorder (ADHD) and has been associated with alterations in the neural orienting and alerting networks. Task-irrelevant stimuli are thus expected to have detrimental effects on the performance of patients with ADHD. Howeve...

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Main Authors: Jana Tegelbeckers, André Brechmann, Carolin Breitling-Ziegler, Bjoern Bonath, Hans-Henning Flechtner, Kerstin Krauel
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-06-01
Series:Frontiers in Human Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fnhum.2022.878994/full
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author Jana Tegelbeckers
Jana Tegelbeckers
André Brechmann
André Brechmann
Carolin Breitling-Ziegler
Bjoern Bonath
Hans-Henning Flechtner
Kerstin Krauel
Kerstin Krauel
author_facet Jana Tegelbeckers
Jana Tegelbeckers
André Brechmann
André Brechmann
Carolin Breitling-Ziegler
Bjoern Bonath
Hans-Henning Flechtner
Kerstin Krauel
Kerstin Krauel
author_sort Jana Tegelbeckers
collection DOAJ
description Distractibility is one of the key features of attention deficit hyperactivity disorder (ADHD) and has been associated with alterations in the neural orienting and alerting networks. Task-irrelevant stimuli are thus expected to have detrimental effects on the performance of patients with ADHD. However, task-irrelevant presentation of novel sounds seems to have the opposite effect and improve subsequent attentional performance particularly in patients with ADHD. Here, we aimed to understand the neural modulations of the attention networks underlying these improvements. Fifty boys (25 with ADHD) participated in a functional magnetic resonance imaging (fMRI) study in which unique (novel) or repeatedly presented (familiar) sounds were placed before a visual flanker task in 2/3 of the trials. We found that presenting any sound improved task performance in all participants, but the underlying neural mechanisms differed for the type of sound. Familiar sounds led to a stronger increase in activity in the left posterior insula in patients with ADHD compared to typically developing peers. Novel sounds led to activations of the fronto-temporoparietal ventral attention network, likewise in ADHD and TD. These changes in signaling by novelty in the right inferior frontal gyrus were directly related to improved response speed showing that neural orienting network activity following novel sounds facilitated subsequent attentional performance. This mechanism of behavioral enhancement by short distractions could potentially be useful for cognitive trainings or homework situations.
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spelling doaj.art-536d9e6a718b47b089e92c726636d3bd2022-12-22T00:35:02ZengFrontiers Media S.A.Frontiers in Human Neuroscience1662-51612022-06-011610.3389/fnhum.2022.878994878994Neural Mechanisms Underlying the Effects of Novel Sounds on Task Performance in Children With and Without ADHDJana Tegelbeckers0Jana Tegelbeckers1André Brechmann2André Brechmann3Carolin Breitling-Ziegler4Bjoern Bonath5Hans-Henning Flechtner6Kerstin Krauel7Kerstin Krauel8Department of Children and Adolescent Psychiatry and Psychotherapy, Otto-von-Guericke-University Magdeburg, Magdeburg, GermanyDepartment of Neuropsychology, Otto-von-Guericke-University Magdeburg, Magdeburg, GermanyCombinatorial Neuroimaging Core Facility, Leibniz Institute for Neurobiology, Magdeburg, GermanyCenter for Behavioral Brain Sciences, Magdeburg, GermanyDepartment of Children and Adolescent Psychiatry and Psychotherapy, Otto-von-Guericke-University Magdeburg, Magdeburg, GermanyDepartment of Children and Adolescent Psychiatry and Psychotherapy, Otto-von-Guericke-University Magdeburg, Magdeburg, GermanyDepartment of Children and Adolescent Psychiatry and Psychotherapy, Otto-von-Guericke-University Magdeburg, Magdeburg, GermanyDepartment of Children and Adolescent Psychiatry and Psychotherapy, Otto-von-Guericke-University Magdeburg, Magdeburg, GermanyCenter for Behavioral Brain Sciences, Magdeburg, GermanyDistractibility is one of the key features of attention deficit hyperactivity disorder (ADHD) and has been associated with alterations in the neural orienting and alerting networks. Task-irrelevant stimuli are thus expected to have detrimental effects on the performance of patients with ADHD. However, task-irrelevant presentation of novel sounds seems to have the opposite effect and improve subsequent attentional performance particularly in patients with ADHD. Here, we aimed to understand the neural modulations of the attention networks underlying these improvements. Fifty boys (25 with ADHD) participated in a functional magnetic resonance imaging (fMRI) study in which unique (novel) or repeatedly presented (familiar) sounds were placed before a visual flanker task in 2/3 of the trials. We found that presenting any sound improved task performance in all participants, but the underlying neural mechanisms differed for the type of sound. Familiar sounds led to a stronger increase in activity in the left posterior insula in patients with ADHD compared to typically developing peers. Novel sounds led to activations of the fronto-temporoparietal ventral attention network, likewise in ADHD and TD. These changes in signaling by novelty in the right inferior frontal gyrus were directly related to improved response speed showing that neural orienting network activity following novel sounds facilitated subsequent attentional performance. This mechanism of behavioral enhancement by short distractions could potentially be useful for cognitive trainings or homework situations.https://www.frontiersin.org/articles/10.3389/fnhum.2022.878994/fullADHD (attention deficit hyperactivity disorder)alertnessdistractionexecutive controlfMRInovelty
spellingShingle Jana Tegelbeckers
Jana Tegelbeckers
André Brechmann
André Brechmann
Carolin Breitling-Ziegler
Bjoern Bonath
Hans-Henning Flechtner
Kerstin Krauel
Kerstin Krauel
Neural Mechanisms Underlying the Effects of Novel Sounds on Task Performance in Children With and Without ADHD
Frontiers in Human Neuroscience
ADHD (attention deficit hyperactivity disorder)
alertness
distraction
executive control
fMRI
novelty
title Neural Mechanisms Underlying the Effects of Novel Sounds on Task Performance in Children With and Without ADHD
title_full Neural Mechanisms Underlying the Effects of Novel Sounds on Task Performance in Children With and Without ADHD
title_fullStr Neural Mechanisms Underlying the Effects of Novel Sounds on Task Performance in Children With and Without ADHD
title_full_unstemmed Neural Mechanisms Underlying the Effects of Novel Sounds on Task Performance in Children With and Without ADHD
title_short Neural Mechanisms Underlying the Effects of Novel Sounds on Task Performance in Children With and Without ADHD
title_sort neural mechanisms underlying the effects of novel sounds on task performance in children with and without adhd
topic ADHD (attention deficit hyperactivity disorder)
alertness
distraction
executive control
fMRI
novelty
url https://www.frontiersin.org/articles/10.3389/fnhum.2022.878994/full
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