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Rhythm in the Premature Neonate Brain: Very Early Processing of Auditory Beat and Meter

The ability to extract rhythmic structure is important for the development of language, music, and social communication. Although previous studies show infants' brains entrain to the periodicities of auditory rhythms and even different metrical interpretations (e.g., groups of two vs three beat...

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Autores principales: Edalati, Mohammadreza, Wallois, Fabrice, Safaie, Javad, Ghostine, Ghida, Kongolo, Guy, Trainor, Laurel J., Moghimi, Sahar
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Society for Neuroscience 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10089239/
https://www.ncbi.nlm.nih.gov/pubmed/36914264
http://dx.doi.org/10.1523/JNEUROSCI.1100-22.2023
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author Edalati, Mohammadreza
Wallois, Fabrice
Safaie, Javad
Ghostine, Ghida
Kongolo, Guy
Trainor, Laurel J.
Moghimi, Sahar
author_facet Edalati, Mohammadreza
Wallois, Fabrice
Safaie, Javad
Ghostine, Ghida
Kongolo, Guy
Trainor, Laurel J.
Moghimi, Sahar
author_sort Edalati, Mohammadreza
collection PubMed
description The ability to extract rhythmic structure is important for the development of language, music, and social communication. Although previous studies show infants' brains entrain to the periodicities of auditory rhythms and even different metrical interpretations (e.g., groups of two vs three beats) of ambiguous rhythms, whether the premature brain tracks beat and meter frequencies has not been explored previously. We used high-resolution electroencephalography while premature infants (n = 19, 5 male; mean age, 32 ± 2.59 weeks gestational age) heard two auditory rhythms in the incubators. We observed selective enhancement of the neural response at both beat- and meter-related frequencies. Further, neural oscillations at the beat and duple (groups of 2) meter were phase aligned with the envelope of the auditory rhythmic stimuli. Comparing the relative power at beat and meter frequencies across stimuli and frequency revealed evidence for selective enhancement of duple meter. This suggests that even at this early stage of development, neural mechanisms for processing auditory rhythms beyond simple sensory coding are present. Our results add to a few previous neuroimaging studies demonstrating discriminative auditory abilities of premature neural networks. Specifically, our results demonstrate the early capacities of the immature neural circuits and networks to code both simple beat and beat grouping (i.e., hierarchical meter) regularities of auditory sequences. Considering the importance of rhythm processing for acquiring language and music, our findings indicate that even before birth, the premature brain is already learning this important aspect of the auditory world in a sophisticated and abstract way. SIGNIFICANCE STATEMENT Processing auditory rhythm is of great neurodevelopmental importance. In an electroencephalography experiment in premature newborns, we found converging evidence that when presented with auditory rhythms, the premature brain encodes multiple periodicities corresponding to beat and beat grouping (meter) frequencies, and even selectively enhances the neural response to meter compared with beat, as in human adults. We also found that the phase of low-frequency neural oscillations aligns to the envelope of the auditory rhythms and that this phenomenon becomes less precise at lower frequencies. These findings demonstrate the initial capacities of the developing brain to code auditory rhythm and the importance of special care to the auditory environment of this vulnerable population during a highly dynamic period of neural development.
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spelling pubmed-100892392023-04-12 Rhythm in the Premature Neonate Brain: Very Early Processing of Auditory Beat and Meter Edalati, Mohammadreza Wallois, Fabrice Safaie, Javad Ghostine, Ghida Kongolo, Guy Trainor, Laurel J. Moghimi, Sahar J Neurosci Research Articles The ability to extract rhythmic structure is important for the development of language, music, and social communication. Although previous studies show infants' brains entrain to the periodicities of auditory rhythms and even different metrical interpretations (e.g., groups of two vs three beats) of ambiguous rhythms, whether the premature brain tracks beat and meter frequencies has not been explored previously. We used high-resolution electroencephalography while premature infants (n = 19, 5 male; mean age, 32 ± 2.59 weeks gestational age) heard two auditory rhythms in the incubators. We observed selective enhancement of the neural response at both beat- and meter-related frequencies. Further, neural oscillations at the beat and duple (groups of 2) meter were phase aligned with the envelope of the auditory rhythmic stimuli. Comparing the relative power at beat and meter frequencies across stimuli and frequency revealed evidence for selective enhancement of duple meter. This suggests that even at this early stage of development, neural mechanisms for processing auditory rhythms beyond simple sensory coding are present. Our results add to a few previous neuroimaging studies demonstrating discriminative auditory abilities of premature neural networks. Specifically, our results demonstrate the early capacities of the immature neural circuits and networks to code both simple beat and beat grouping (i.e., hierarchical meter) regularities of auditory sequences. Considering the importance of rhythm processing for acquiring language and music, our findings indicate that even before birth, the premature brain is already learning this important aspect of the auditory world in a sophisticated and abstract way. SIGNIFICANCE STATEMENT Processing auditory rhythm is of great neurodevelopmental importance. In an electroencephalography experiment in premature newborns, we found converging evidence that when presented with auditory rhythms, the premature brain encodes multiple periodicities corresponding to beat and beat grouping (meter) frequencies, and even selectively enhances the neural response to meter compared with beat, as in human adults. We also found that the phase of low-frequency neural oscillations aligns to the envelope of the auditory rhythms and that this phenomenon becomes less precise at lower frequencies. These findings demonstrate the initial capacities of the developing brain to code auditory rhythm and the importance of special care to the auditory environment of this vulnerable population during a highly dynamic period of neural development. Society for Neuroscience 2023-04-12 /pmc/articles/PMC10089239/ /pubmed/36914264 http://dx.doi.org/10.1523/JNEUROSCI.1100-22.2023 Text en Copyright © 2023 Edalati et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Articles
Edalati, Mohammadreza
Wallois, Fabrice
Safaie, Javad
Ghostine, Ghida
Kongolo, Guy
Trainor, Laurel J.
Moghimi, Sahar
Rhythm in the Premature Neonate Brain: Very Early Processing of Auditory Beat and Meter
title Rhythm in the Premature Neonate Brain: Very Early Processing of Auditory Beat and Meter
title_full Rhythm in the Premature Neonate Brain: Very Early Processing of Auditory Beat and Meter
title_fullStr Rhythm in the Premature Neonate Brain: Very Early Processing of Auditory Beat and Meter
title_full_unstemmed Rhythm in the Premature Neonate Brain: Very Early Processing of Auditory Beat and Meter
title_short Rhythm in the Premature Neonate Brain: Very Early Processing of Auditory Beat and Meter
title_sort rhythm in the premature neonate brain: very early processing of auditory beat and meter
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10089239/
https://www.ncbi.nlm.nih.gov/pubmed/36914264
http://dx.doi.org/10.1523/JNEUROSCI.1100-22.2023
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