Altered brain network topology in children with auditory processing disorder: A resting-state multi-echo fMRI study

Children with auditory processing disorder (APD) experience hearing difficulties, particularly in the presence of competing sounds, despite having normal audiograms. There is considerable debate on whether APD symptoms originate from bottom-up (e.g., auditory sensory processing) and/or top-down proc...

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Main Authors: Ashkan Alvand, Abin Kuruvilla-Mathew, Ian J. Kirk, Reece P. Roberts, Mangor Pedersen, Suzanne C. Purdy
Format: Article
Language:English
Published: Elsevier 2022-01-01
Series:NeuroImage: Clinical
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2213158222002042
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author Ashkan Alvand
Abin Kuruvilla-Mathew
Ian J. Kirk
Reece P. Roberts
Mangor Pedersen
Suzanne C. Purdy
author_facet Ashkan Alvand
Abin Kuruvilla-Mathew
Ian J. Kirk
Reece P. Roberts
Mangor Pedersen
Suzanne C. Purdy
author_sort Ashkan Alvand
collection DOAJ
description Children with auditory processing disorder (APD) experience hearing difficulties, particularly in the presence of competing sounds, despite having normal audiograms. There is considerable debate on whether APD symptoms originate from bottom-up (e.g., auditory sensory processing) and/or top-down processing (e.g., cognitive, language, memory). A related issue is that little is known about whether functional brain network topology is altered in APD. Therefore, we used resting-state functional magnetic resonance imaging data to investigate the functional brain network organization of 57 children from 8 to 14 years old, diagnosed with APD (n = 28) and without hearing difficulties (healthy control, HC; n = 29). We applied complex network analysis using graph theory to assess the whole-brain integration and segregation of functional networks and brain hub architecture. Our results showed children with APD and HC have similar global network properties –i.e., an average of all brain regions– and modular organization. Still, the APD group showed different hub architecture in default mode-ventral attention, somatomotor and frontoparietal-dorsal attention modules. At the nodal level –i.e., single-brain regions–, we observed decreased participation coefficient (PC – a measure quantifying the diversity of between-network connectivity) in auditory cortical regions in APD, including bilateral superior temporal gyrus and left middle temporal gyrus. Beyond auditory regions, PC was also decreased in APD in bilateral posterior temporo-occipital cortices, left intraparietal sulcus, and right posterior insular cortex. Correlation analysis suggested a positive association between PC in the left parahippocampal gyrus and the listening-in-spatialized-noise -sentences task where APD children were engaged in auditory perception. In conclusion, our findings provide evidence of altered brain network organization in children with APD, specific to auditory networks, and shed new light on the neural systems underlying children's listening difficulties.
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spelling doaj.art-7d6530670bcb43ec81135ce1812730762022-12-22T02:48:37ZengElsevierNeuroImage: Clinical2213-15822022-01-0135103139Altered brain network topology in children with auditory processing disorder: A resting-state multi-echo fMRI studyAshkan Alvand0Abin Kuruvilla-Mathew1Ian J. Kirk2Reece P. Roberts3Mangor Pedersen4Suzanne C. Purdy5School of Psychology, Faculty of Science, The University of Auckland, Auckland, New Zealand; Eisdell Moore Centre, Auckland, New Zealand; Corresponding author at: School of Psychology, Faculty of Science, The University of Auckland, Auckland, New Zealand.School of Psychology, Faculty of Science, The University of Auckland, Auckland, New Zealand; Eisdell Moore Centre, Auckland, New ZealandSchool of Psychology, Faculty of Science, The University of Auckland, Auckland, New Zealand; Eisdell Moore Centre, Auckland, New Zealand; Centre for Brain Research, The University of Auckland, Auckland, New ZealandSchool of Psychology, Faculty of Science, The University of Auckland, Auckland, New Zealand; Centre for Brain Research, The University of Auckland, Auckland, New ZealandSchool of Psychology and Neuroscience, Auckland University of Technology, Auckland, New ZealandSchool of Psychology, Faculty of Science, The University of Auckland, Auckland, New Zealand; Eisdell Moore Centre, Auckland, New Zealand; Centre for Brain Research, The University of Auckland, Auckland, New ZealandChildren with auditory processing disorder (APD) experience hearing difficulties, particularly in the presence of competing sounds, despite having normal audiograms. There is considerable debate on whether APD symptoms originate from bottom-up (e.g., auditory sensory processing) and/or top-down processing (e.g., cognitive, language, memory). A related issue is that little is known about whether functional brain network topology is altered in APD. Therefore, we used resting-state functional magnetic resonance imaging data to investigate the functional brain network organization of 57 children from 8 to 14 years old, diagnosed with APD (n = 28) and without hearing difficulties (healthy control, HC; n = 29). We applied complex network analysis using graph theory to assess the whole-brain integration and segregation of functional networks and brain hub architecture. Our results showed children with APD and HC have similar global network properties –i.e., an average of all brain regions– and modular organization. Still, the APD group showed different hub architecture in default mode-ventral attention, somatomotor and frontoparietal-dorsal attention modules. At the nodal level –i.e., single-brain regions–, we observed decreased participation coefficient (PC – a measure quantifying the diversity of between-network connectivity) in auditory cortical regions in APD, including bilateral superior temporal gyrus and left middle temporal gyrus. Beyond auditory regions, PC was also decreased in APD in bilateral posterior temporo-occipital cortices, left intraparietal sulcus, and right posterior insular cortex. Correlation analysis suggested a positive association between PC in the left parahippocampal gyrus and the listening-in-spatialized-noise -sentences task where APD children were engaged in auditory perception. In conclusion, our findings provide evidence of altered brain network organization in children with APD, specific to auditory networks, and shed new light on the neural systems underlying children's listening difficulties.http://www.sciencedirect.com/science/article/pii/S2213158222002042Auditory processing disorderHubFunctional connectivityGraph theoryListening difficultiesfMRI
spellingShingle Ashkan Alvand
Abin Kuruvilla-Mathew
Ian J. Kirk
Reece P. Roberts
Mangor Pedersen
Suzanne C. Purdy
Altered brain network topology in children with auditory processing disorder: A resting-state multi-echo fMRI study
NeuroImage: Clinical
Auditory processing disorder
Hub
Functional connectivity
Graph theory
Listening difficulties
fMRI
title Altered brain network topology in children with auditory processing disorder: A resting-state multi-echo fMRI study
title_full Altered brain network topology in children with auditory processing disorder: A resting-state multi-echo fMRI study
title_fullStr Altered brain network topology in children with auditory processing disorder: A resting-state multi-echo fMRI study
title_full_unstemmed Altered brain network topology in children with auditory processing disorder: A resting-state multi-echo fMRI study
title_short Altered brain network topology in children with auditory processing disorder: A resting-state multi-echo fMRI study
title_sort altered brain network topology in children with auditory processing disorder a resting state multi echo fmri study
topic Auditory processing disorder
Hub
Functional connectivity
Graph theory
Listening difficulties
fMRI
url http://www.sciencedirect.com/science/article/pii/S2213158222002042
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