Preterm neonates distinguish rhythm violation through a hierarchy of cortical processing

Rhythm is a fundamental component of the auditory world, present even during the prenatal life. While there is evidence that some auditory capacities are already present before birth, whether and how the premature neural networks process auditory rhythm is yet not known. We investigated the neural r...

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Main Authors: Mohammadreza Edalati, Mahdi Mahmoudzadeh, Ghida Ghostine, Guy Kongolo, Javad Safaie, Fabrice Wallois, Sahar Moghimi
Format: Article
Language:English
Published: Elsevier 2022-12-01
Series:Developmental Cognitive Neuroscience
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S1878929322001116
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author Mohammadreza Edalati
Mahdi Mahmoudzadeh
Ghida Ghostine
Guy Kongolo
Javad Safaie
Fabrice Wallois
Sahar Moghimi
author_facet Mohammadreza Edalati
Mahdi Mahmoudzadeh
Ghida Ghostine
Guy Kongolo
Javad Safaie
Fabrice Wallois
Sahar Moghimi
author_sort Mohammadreza Edalati
collection DOAJ
description Rhythm is a fundamental component of the auditory world, present even during the prenatal life. While there is evidence that some auditory capacities are already present before birth, whether and how the premature neural networks process auditory rhythm is yet not known. We investigated the neural response of premature neonates at 30–34 weeks gestational age to violations from rhythmic regularities in an auditory sequence using high-resolution electroencephalography and event-related potentials. Unpredicted rhythm violations elicited a fronto-central mismatch response, indicating that the premature neonates detected the rhythmic regularities. Next, we examined the cortical effective connectivity underlying the elicited mismatch response using dynamic causal modeling. We examined the connectivity between cortical sources using a set of 16 generative models that embedded alternate hypotheses about the role of the frontal cortex as well as backward fronto-temporal connection. Our results demonstrated that the processing of rhythm violations was not limited to the primary auditory areas, and as in the case of adults, encompassed a hierarchy of temporo-frontal cortical structures. The result also emphasized the importance of top-down (backward) projections from the frontal cortex in explaining the mismatch response. Our findings demonstrate a sophisticated cortical structure underlying predictive rhythm processing at the onset of the thalamocortical and cortico-cortical circuits, two months before term.
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spelling doaj.art-9adcd667aae24c74a08064b8ad17a1b32022-12-22T03:01:59ZengElsevierDevelopmental Cognitive Neuroscience1878-92932022-12-0158101168Preterm neonates distinguish rhythm violation through a hierarchy of cortical processingMohammadreza Edalati0Mahdi Mahmoudzadeh1Ghida Ghostine2Guy Kongolo3Javad Safaie4Fabrice Wallois5Sahar Moghimi6Inserm UMR1105, Groupe de Recherches sur l′Analyse Multimodale de la Fonction Cérébrale, CURS, Avenue Laennec, 80054 Amiens Cedex, France; Electrical Engineering Department, Ferdowsi University of Mashhad, 9177948974 Mashhad, IranInserm UMR1105, Groupe de Recherches sur l′Analyse Multimodale de la Fonction Cérébrale, CURS, Avenue Laennec, 80054 Amiens Cedex, FranceInserm UMR1105, Groupe de Recherches sur l′Analyse Multimodale de la Fonction Cérébrale, CURS, Avenue Laennec, 80054 Amiens Cedex, FranceInserm UMR1105, Groupe de Recherches sur l′Analyse Multimodale de la Fonction Cérébrale, CURS, Avenue Laennec, 80054 Amiens Cedex, FranceElectrical Engineering Department, Ferdowsi University of Mashhad, 9177948974 Mashhad, IranInserm UMR1105, Groupe de Recherches sur l′Analyse Multimodale de la Fonction Cérébrale, CURS, Avenue Laennec, 80054 Amiens Cedex, France; Inserm UMR1105, EFSN Pédiatriques, CHU Amiens sud, Avenue Laennec, 80054 Amiens Cedex, FranceInserm UMR1105, Groupe de Recherches sur l′Analyse Multimodale de la Fonction Cérébrale, CURS, Avenue Laennec, 80054 Amiens Cedex, France; Corresponding author at: Inserm UMR1105, Groupe de Recherches sur l′Analyse Multimodale de la Fonction Cérébrale, CURS, Avenue Laennec, 80054 Amiens Cedex, France.Rhythm is a fundamental component of the auditory world, present even during the prenatal life. While there is evidence that some auditory capacities are already present before birth, whether and how the premature neural networks process auditory rhythm is yet not known. We investigated the neural response of premature neonates at 30–34 weeks gestational age to violations from rhythmic regularities in an auditory sequence using high-resolution electroencephalography and event-related potentials. Unpredicted rhythm violations elicited a fronto-central mismatch response, indicating that the premature neonates detected the rhythmic regularities. Next, we examined the cortical effective connectivity underlying the elicited mismatch response using dynamic causal modeling. We examined the connectivity between cortical sources using a set of 16 generative models that embedded alternate hypotheses about the role of the frontal cortex as well as backward fronto-temporal connection. Our results demonstrated that the processing of rhythm violations was not limited to the primary auditory areas, and as in the case of adults, encompassed a hierarchy of temporo-frontal cortical structures. The result also emphasized the importance of top-down (backward) projections from the frontal cortex in explaining the mismatch response. Our findings demonstrate a sophisticated cortical structure underlying predictive rhythm processing at the onset of the thalamocortical and cortico-cortical circuits, two months before term.http://www.sciencedirect.com/science/article/pii/S1878929322001116Premature human brainRhythmElectroencephalographyDynamic causal modelingPredictive coding
spellingShingle Mohammadreza Edalati
Mahdi Mahmoudzadeh
Ghida Ghostine
Guy Kongolo
Javad Safaie
Fabrice Wallois
Sahar Moghimi
Preterm neonates distinguish rhythm violation through a hierarchy of cortical processing
Developmental Cognitive Neuroscience
Premature human brain
Rhythm
Electroencephalography
Dynamic causal modeling
Predictive coding
title Preterm neonates distinguish rhythm violation through a hierarchy of cortical processing
title_full Preterm neonates distinguish rhythm violation through a hierarchy of cortical processing
title_fullStr Preterm neonates distinguish rhythm violation through a hierarchy of cortical processing
title_full_unstemmed Preterm neonates distinguish rhythm violation through a hierarchy of cortical processing
title_short Preterm neonates distinguish rhythm violation through a hierarchy of cortical processing
title_sort preterm neonates distinguish rhythm violation through a hierarchy of cortical processing
topic Premature human brain
Rhythm
Electroencephalography
Dynamic causal modeling
Predictive coding
url http://www.sciencedirect.com/science/article/pii/S1878929322001116
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