Timing of phase‐amplitude coupling is essential for neuronal and functional maturation of audiovisual integration in adolescents

Abstract Objective The ability to integrate audiovisual information matures late in adolescents, but its neuronal mechanism is still unknown. Recent studies showed that phase‐amplitude coupling (PAC) of neuronal oscillations, which is defined as the modulation of high‐frequency amplitude by low‐freq...

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Main Authors: Takefumi Ohki, Takeru Matsuda, Atsuko Gunji, Yuichi Takei, Ryusuke Sakuma, Yuu Kaneko, Masumi Inagaki, Takashi Hanakawa, Kazuhiro Ueda, Masato Fukuda, Kazuo Hiraki
Format: Article
Language:English
Published: Wiley 2020-06-01
Series:Brain and Behavior
Subjects:
Online Access:https://doi.org/10.1002/brb3.1635
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author Takefumi Ohki
Takeru Matsuda
Atsuko Gunji
Yuichi Takei
Ryusuke Sakuma
Yuu Kaneko
Masumi Inagaki
Takashi Hanakawa
Kazuhiro Ueda
Masato Fukuda
Kazuo Hiraki
author_facet Takefumi Ohki
Takeru Matsuda
Atsuko Gunji
Yuichi Takei
Ryusuke Sakuma
Yuu Kaneko
Masumi Inagaki
Takashi Hanakawa
Kazuhiro Ueda
Masato Fukuda
Kazuo Hiraki
author_sort Takefumi Ohki
collection DOAJ
description Abstract Objective The ability to integrate audiovisual information matures late in adolescents, but its neuronal mechanism is still unknown. Recent studies showed that phase‐amplitude coupling (PAC) of neuronal oscillations, which is defined as the modulation of high‐frequency amplitude by low‐frequency phase, is associated with audiovisual integration in adults. Thus, we investigated how PAC develops in adolescents and whether it is related to the functional maturation of audiovisual integration. In particular, we focused on the timing of PAC (or the coupling phase), which is defined as the low‐frequency phase with maximum high‐frequency amplitude. Methods Using magnetoencephalography (MEG) on 15 adults and 14 adolescents while they performed an audiovisual speech integration task, we examined PAC in association cortexes with a trial‐by‐trial analysis. Results Whereas delta‐beta coupling was consistently observed in both adults and adolescents, we found that the timing of delta‐beta PAC was delayed by 20–40 milliseconds in adolescents compared with adults. In addition, a logistic regression analysis revealed that the task performance improves as the timing of delta‐beta PAC in the right temporal pole (TP) got closer to the trough position (180 degrees). Conclusion These results suggest that the timing of PAC is essential for binding audiovisual information and underlies the developmental process in adolescents.
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spelling doaj.art-c16fcba8f79d4a759045ba5f2c0d45982022-12-21T22:46:03ZengWileyBrain and Behavior2162-32792020-06-01106n/an/a10.1002/brb3.1635Timing of phase‐amplitude coupling is essential for neuronal and functional maturation of audiovisual integration in adolescentsTakefumi Ohki0Takeru Matsuda1Atsuko Gunji2Yuichi Takei3Ryusuke Sakuma4Yuu Kaneko5Masumi Inagaki6Takashi Hanakawa7Kazuhiro Ueda8Masato Fukuda9Kazuo Hiraki10Graduate School of Arts and Sciences University of Tokyo Tokyo JapanDepartment of Mathematical Informatics Graduate School of Information Science and Technology University of Tokyo Tokyo JapanDepartment of Neurosurgery Osaka University Graduate School of Medicine Suita JapanDepartment of Psychiatry and Neuroscience Gunma University Graduate School of Medicine Gunma JapanDepartment of Developmental Disorders National Institute of Mental Health National Centre of Neurology and Psychiatry Tokyo JapanDepartment of Neurosurgery National Center Hospital National Centre of Neurology and Psychiatry Tokyo JapanDepartment of Developmental Disorders National Institute of Mental Health National Centre of Neurology and Psychiatry Tokyo JapanDepartment of Advanced Neuroimaging Integrative Brain Imaging Center National Centre of Neurology and Psychiatry Tokyo JapanGraduate School of Arts and Sciences University of Tokyo Tokyo JapanDepartment of Psychiatry and Neuroscience Gunma University Graduate School of Medicine Gunma JapanGraduate School of Arts and Sciences University of Tokyo Tokyo JapanAbstract Objective The ability to integrate audiovisual information matures late in adolescents, but its neuronal mechanism is still unknown. Recent studies showed that phase‐amplitude coupling (PAC) of neuronal oscillations, which is defined as the modulation of high‐frequency amplitude by low‐frequency phase, is associated with audiovisual integration in adults. Thus, we investigated how PAC develops in adolescents and whether it is related to the functional maturation of audiovisual integration. In particular, we focused on the timing of PAC (or the coupling phase), which is defined as the low‐frequency phase with maximum high‐frequency amplitude. Methods Using magnetoencephalography (MEG) on 15 adults and 14 adolescents while they performed an audiovisual speech integration task, we examined PAC in association cortexes with a trial‐by‐trial analysis. Results Whereas delta‐beta coupling was consistently observed in both adults and adolescents, we found that the timing of delta‐beta PAC was delayed by 20–40 milliseconds in adolescents compared with adults. In addition, a logistic regression analysis revealed that the task performance improves as the timing of delta‐beta PAC in the right temporal pole (TP) got closer to the trough position (180 degrees). Conclusion These results suggest that the timing of PAC is essential for binding audiovisual information and underlies the developmental process in adolescents.https://doi.org/10.1002/brb3.1635adolescenceaudiovisual integrationdelta‐beta couplingneuronal oscillationspeech
spellingShingle Takefumi Ohki
Takeru Matsuda
Atsuko Gunji
Yuichi Takei
Ryusuke Sakuma
Yuu Kaneko
Masumi Inagaki
Takashi Hanakawa
Kazuhiro Ueda
Masato Fukuda
Kazuo Hiraki
Timing of phase‐amplitude coupling is essential for neuronal and functional maturation of audiovisual integration in adolescents
Brain and Behavior
adolescence
audiovisual integration
delta‐beta coupling
neuronal oscillation
speech
title Timing of phase‐amplitude coupling is essential for neuronal and functional maturation of audiovisual integration in adolescents
title_full Timing of phase‐amplitude coupling is essential for neuronal and functional maturation of audiovisual integration in adolescents
title_fullStr Timing of phase‐amplitude coupling is essential for neuronal and functional maturation of audiovisual integration in adolescents
title_full_unstemmed Timing of phase‐amplitude coupling is essential for neuronal and functional maturation of audiovisual integration in adolescents
title_short Timing of phase‐amplitude coupling is essential for neuronal and functional maturation of audiovisual integration in adolescents
title_sort timing of phase amplitude coupling is essential for neuronal and functional maturation of audiovisual integration in adolescents
topic adolescence
audiovisual integration
delta‐beta coupling
neuronal oscillation
speech
url https://doi.org/10.1002/brb3.1635
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