Cargando…

Genuine cross-frequency coupling networks in human resting-state electrophysiological recordings

Phase synchronization of neuronal oscillations in specific frequency bands coordinates anatomically distributed neuronal processing and communication. Typically, oscillations and synchronization take place concurrently in many distinct frequencies, which serve separate computational roles in cogniti...

Descripción completa

Detalles Bibliográficos
Autores principales: Siebenhühner, Felix, Wang, Sheng H., Arnulfo, Gabriele, Lampinen, Anna, Nobili, Lino, Palva, J. Matias, Palva, Satu
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7233600/
https://www.ncbi.nlm.nih.gov/pubmed/32374723
http://dx.doi.org/10.1371/journal.pbio.3000685
_version_ 1783535570645942272
author Siebenhühner, Felix
Wang, Sheng H.
Arnulfo, Gabriele
Lampinen, Anna
Nobili, Lino
Palva, J. Matias
Palva, Satu
author_facet Siebenhühner, Felix
Wang, Sheng H.
Arnulfo, Gabriele
Lampinen, Anna
Nobili, Lino
Palva, J. Matias
Palva, Satu
author_sort Siebenhühner, Felix
collection PubMed
description Phase synchronization of neuronal oscillations in specific frequency bands coordinates anatomically distributed neuronal processing and communication. Typically, oscillations and synchronization take place concurrently in many distinct frequencies, which serve separate computational roles in cognitive functions. While within-frequency phase synchronization has been studied extensively, less is known about the mechanisms that govern neuronal processing distributed across frequencies and brain regions. Such integration of processing between frequencies could be achieved via cross-frequency coupling (CFC), either by phase–amplitude coupling (PAC) or by n:m-cross–frequency phase synchrony (CFS). So far, studies have mostly focused on local CFC in individual brain regions, whereas the presence and functional organization of CFC between brain areas have remained largely unknown. We posit that interareal CFC may be essential for large-scale coordination of neuronal activity and investigate here whether genuine CFC networks are present in human resting-state (RS) brain activity. To assess the functional organization of CFC networks, we identified brain-wide CFC networks at mesoscale resolution from stereoelectroencephalography (SEEG) and at macroscale resolution from source-reconstructed magnetoencephalography (MEG) data. We developed a novel, to our knowledge, graph-theoretical method to distinguish genuine CFC from spurious CFC that may arise from nonsinusoidal signals ubiquitous in neuronal activity. We show that genuine interareal CFC is present in human RS activity in both SEEG and MEG data. Both CFS and PAC networks coupled theta and alpha oscillations with higher frequencies in large-scale networks connecting anterior and posterior brain regions. CFS and PAC networks had distinct spectral patterns and opposing distribution of low- and high-frequency network hubs, implying that they constitute distinct CFC mechanisms. The strength of CFS networks was also predictive of cognitive performance in a separate neuropsychological assessment. In conclusion, these results provide evidence for interareal CFS and PAC being 2 distinct mechanisms for coupling oscillations across frequencies in large-scale brain networks.
format Online
Article
Text
id pubmed-7233600
institution National Center for Biotechnology Information
language English
publishDate 2020
publisher Public Library of Science
record_format MEDLINE/PubMed
spelling pubmed-72336002020-06-02 Genuine cross-frequency coupling networks in human resting-state electrophysiological recordings Siebenhühner, Felix Wang, Sheng H. Arnulfo, Gabriele Lampinen, Anna Nobili, Lino Palva, J. Matias Palva, Satu PLoS Biol Research Article Phase synchronization of neuronal oscillations in specific frequency bands coordinates anatomically distributed neuronal processing and communication. Typically, oscillations and synchronization take place concurrently in many distinct frequencies, which serve separate computational roles in cognitive functions. While within-frequency phase synchronization has been studied extensively, less is known about the mechanisms that govern neuronal processing distributed across frequencies and brain regions. Such integration of processing between frequencies could be achieved via cross-frequency coupling (CFC), either by phase–amplitude coupling (PAC) or by n:m-cross–frequency phase synchrony (CFS). So far, studies have mostly focused on local CFC in individual brain regions, whereas the presence and functional organization of CFC between brain areas have remained largely unknown. We posit that interareal CFC may be essential for large-scale coordination of neuronal activity and investigate here whether genuine CFC networks are present in human resting-state (RS) brain activity. To assess the functional organization of CFC networks, we identified brain-wide CFC networks at mesoscale resolution from stereoelectroencephalography (SEEG) and at macroscale resolution from source-reconstructed magnetoencephalography (MEG) data. We developed a novel, to our knowledge, graph-theoretical method to distinguish genuine CFC from spurious CFC that may arise from nonsinusoidal signals ubiquitous in neuronal activity. We show that genuine interareal CFC is present in human RS activity in both SEEG and MEG data. Both CFS and PAC networks coupled theta and alpha oscillations with higher frequencies in large-scale networks connecting anterior and posterior brain regions. CFS and PAC networks had distinct spectral patterns and opposing distribution of low- and high-frequency network hubs, implying that they constitute distinct CFC mechanisms. The strength of CFS networks was also predictive of cognitive performance in a separate neuropsychological assessment. In conclusion, these results provide evidence for interareal CFS and PAC being 2 distinct mechanisms for coupling oscillations across frequencies in large-scale brain networks. Public Library of Science 2020-05-06 /pmc/articles/PMC7233600/ /pubmed/32374723 http://dx.doi.org/10.1371/journal.pbio.3000685 Text en © 2020 Siebenhühner et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Siebenhühner, Felix
Wang, Sheng H.
Arnulfo, Gabriele
Lampinen, Anna
Nobili, Lino
Palva, J. Matias
Palva, Satu
Genuine cross-frequency coupling networks in human resting-state electrophysiological recordings
title Genuine cross-frequency coupling networks in human resting-state electrophysiological recordings
title_full Genuine cross-frequency coupling networks in human resting-state electrophysiological recordings
title_fullStr Genuine cross-frequency coupling networks in human resting-state electrophysiological recordings
title_full_unstemmed Genuine cross-frequency coupling networks in human resting-state electrophysiological recordings
title_short Genuine cross-frequency coupling networks in human resting-state electrophysiological recordings
title_sort genuine cross-frequency coupling networks in human resting-state electrophysiological recordings
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7233600/
https://www.ncbi.nlm.nih.gov/pubmed/32374723
http://dx.doi.org/10.1371/journal.pbio.3000685
work_keys_str_mv AT siebenhuhnerfelix genuinecrossfrequencycouplingnetworksinhumanrestingstateelectrophysiologicalrecordings
AT wangshengh genuinecrossfrequencycouplingnetworksinhumanrestingstateelectrophysiologicalrecordings
AT arnulfogabriele genuinecrossfrequencycouplingnetworksinhumanrestingstateelectrophysiologicalrecordings
AT lampinenanna genuinecrossfrequencycouplingnetworksinhumanrestingstateelectrophysiologicalrecordings
AT nobililino genuinecrossfrequencycouplingnetworksinhumanrestingstateelectrophysiologicalrecordings
AT palvajmatias genuinecrossfrequencycouplingnetworksinhumanrestingstateelectrophysiologicalrecordings
AT palvasatu genuinecrossfrequencycouplingnetworksinhumanrestingstateelectrophysiologicalrecordings