Cargando…

Ultralow-frequency neural entrainment to pain

Nervous systems exploit regularities in the sensory environment to predict sensory input, adjust behavior, and thereby maximize fitness. Entrainment of neural oscillations allows retaining temporal regularities of sensory information, a prerequisite for prediction. Entrainment has been extensively d...

Descripción completa

Detalles Bibliográficos
Autores principales: Guo, Yifei, Bufacchi, Rory John, Novembre, Giacomo, Kilintari, Marina, Moayedi, Massieh, Hu, Li, Iannetti, Gian Domenico
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7179945/
https://www.ncbi.nlm.nih.gov/pubmed/32282798
http://dx.doi.org/10.1371/journal.pbio.3000491
_version_ 1783525733622087680
author Guo, Yifei
Bufacchi, Rory John
Novembre, Giacomo
Kilintari, Marina
Moayedi, Massieh
Hu, Li
Iannetti, Gian Domenico
author_facet Guo, Yifei
Bufacchi, Rory John
Novembre, Giacomo
Kilintari, Marina
Moayedi, Massieh
Hu, Li
Iannetti, Gian Domenico
author_sort Guo, Yifei
collection PubMed
description Nervous systems exploit regularities in the sensory environment to predict sensory input, adjust behavior, and thereby maximize fitness. Entrainment of neural oscillations allows retaining temporal regularities of sensory information, a prerequisite for prediction. Entrainment has been extensively described at the frequencies of periodic inputs most commonly present in visual and auditory landscapes (e.g., >0.5 Hz). An open question is whether neural entrainment also occurs for regularities at much longer timescales. Here, we exploited the fact that the temporal dynamics of thermal stimuli in natural environment can unfold very slowly. We show that ultralow-frequency neural oscillations preserved a long-lasting trace of sensory information through neural entrainment to periodic thermo-nociceptive input as low as 0.1 Hz. Importantly, revealing the functional significance of this phenomenon, both power and phase of the entrainment predicted individual pain sensitivity. In contrast, periodic auditory input at the same ultralow frequency did not entrain ultralow-frequency oscillations. These results demonstrate that a functionally significant neural entrainment can occur at temporal scales far longer than those commonly explored. The non-supramodal nature of our results suggests that ultralow-frequency entrainment might be tuned to the temporal scale of the statistical regularities characteristic of different sensory modalities.
format Online
Article
Text
id pubmed-7179945
institution National Center for Biotechnology Information
language English
publishDate 2020
publisher Public Library of Science
record_format MEDLINE/PubMed
spelling pubmed-71799452020-05-05 Ultralow-frequency neural entrainment to pain Guo, Yifei Bufacchi, Rory John Novembre, Giacomo Kilintari, Marina Moayedi, Massieh Hu, Li Iannetti, Gian Domenico PLoS Biol Research Article Nervous systems exploit regularities in the sensory environment to predict sensory input, adjust behavior, and thereby maximize fitness. Entrainment of neural oscillations allows retaining temporal regularities of sensory information, a prerequisite for prediction. Entrainment has been extensively described at the frequencies of periodic inputs most commonly present in visual and auditory landscapes (e.g., >0.5 Hz). An open question is whether neural entrainment also occurs for regularities at much longer timescales. Here, we exploited the fact that the temporal dynamics of thermal stimuli in natural environment can unfold very slowly. We show that ultralow-frequency neural oscillations preserved a long-lasting trace of sensory information through neural entrainment to periodic thermo-nociceptive input as low as 0.1 Hz. Importantly, revealing the functional significance of this phenomenon, both power and phase of the entrainment predicted individual pain sensitivity. In contrast, periodic auditory input at the same ultralow frequency did not entrain ultralow-frequency oscillations. These results demonstrate that a functionally significant neural entrainment can occur at temporal scales far longer than those commonly explored. The non-supramodal nature of our results suggests that ultralow-frequency entrainment might be tuned to the temporal scale of the statistical regularities characteristic of different sensory modalities. Public Library of Science 2020-04-13 /pmc/articles/PMC7179945/ /pubmed/32282798 http://dx.doi.org/10.1371/journal.pbio.3000491 Text en © 2020 Guo 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
Guo, Yifei
Bufacchi, Rory John
Novembre, Giacomo
Kilintari, Marina
Moayedi, Massieh
Hu, Li
Iannetti, Gian Domenico
Ultralow-frequency neural entrainment to pain
title Ultralow-frequency neural entrainment to pain
title_full Ultralow-frequency neural entrainment to pain
title_fullStr Ultralow-frequency neural entrainment to pain
title_full_unstemmed Ultralow-frequency neural entrainment to pain
title_short Ultralow-frequency neural entrainment to pain
title_sort ultralow-frequency neural entrainment to pain
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7179945/
https://www.ncbi.nlm.nih.gov/pubmed/32282798
http://dx.doi.org/10.1371/journal.pbio.3000491
work_keys_str_mv AT guoyifei ultralowfrequencyneuralentrainmenttopain
AT bufacchiroryjohn ultralowfrequencyneuralentrainmenttopain
AT novembregiacomo ultralowfrequencyneuralentrainmenttopain
AT kilintarimarina ultralowfrequencyneuralentrainmenttopain
AT moayedimassieh ultralowfrequencyneuralentrainmenttopain
AT huli ultralowfrequencyneuralentrainmenttopain
AT iannettigiandomenico ultralowfrequencyneuralentrainmenttopain