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Spontaneous neuronal oscillations in the human insula are hierarchically organized traveling waves

The insula plays a fundamental role in a wide range of adaptive human behaviors, but its electrophysiological dynamics are poorly understood. Here, we used human intracranial electroencephalographic recordings to investigate the electrophysiological properties and hierarchical organization of sponta...

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Autores principales: Das, Anup, Myers, John, Mathura, Raissa, Shofty, Ben, Metzger, Brian A, Bijanki, Kelly, Wu, Chengyuan, Jacobs, Joshua, Sheth, Sameer A
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9200407/
https://www.ncbi.nlm.nih.gov/pubmed/35616527
http://dx.doi.org/10.7554/eLife.76702
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author Das, Anup
Myers, John
Mathura, Raissa
Shofty, Ben
Metzger, Brian A
Bijanki, Kelly
Wu, Chengyuan
Jacobs, Joshua
Sheth, Sameer A
author_facet Das, Anup
Myers, John
Mathura, Raissa
Shofty, Ben
Metzger, Brian A
Bijanki, Kelly
Wu, Chengyuan
Jacobs, Joshua
Sheth, Sameer A
author_sort Das, Anup
collection PubMed
description The insula plays a fundamental role in a wide range of adaptive human behaviors, but its electrophysiological dynamics are poorly understood. Here, we used human intracranial electroencephalographic recordings to investigate the electrophysiological properties and hierarchical organization of spontaneous neuronal oscillations within the insula. We analyzed the neuronal oscillations of the insula directly and found that rhythms in the theta and beta frequency oscillations are widespread and spontaneously present. These oscillations are largely organized along the anterior–posterior (AP) axis of the insula. Both the left and right insula showed anterior-­to-posterior decreasing gradients for the power of oscillations in the beta frequency band. The left insula also showed a posterior-to-anterior decreasing frequency gradient and an anterior-to-posterior decreasing power gradient in the theta frequency band. In addition to measuring the power of these oscillations, we also examined the phase of these signals across simultaneous recording channels and found that the insula oscillations in the theta and beta bands are traveling waves. The strength of the traveling waves in each frequency was positively correlated with the amplitude of each oscillation. However, the theta and beta traveling waves were uncoupled to each other in terms of phase and amplitude, which suggested that insular traveling waves in the theta and beta bands operate independently. Our findings provide new insights into the spatiotemporal dynamics and hierarchical organization of neuronal oscillations within the insula, which, given its rich connectivity with widespread cortical regions, indicates that oscillations and traveling waves have an important role in intrainsular and interinsular communications.
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spelling pubmed-92004072022-06-16 Spontaneous neuronal oscillations in the human insula are hierarchically organized traveling waves Das, Anup Myers, John Mathura, Raissa Shofty, Ben Metzger, Brian A Bijanki, Kelly Wu, Chengyuan Jacobs, Joshua Sheth, Sameer A eLife Neuroscience The insula plays a fundamental role in a wide range of adaptive human behaviors, but its electrophysiological dynamics are poorly understood. Here, we used human intracranial electroencephalographic recordings to investigate the electrophysiological properties and hierarchical organization of spontaneous neuronal oscillations within the insula. We analyzed the neuronal oscillations of the insula directly and found that rhythms in the theta and beta frequency oscillations are widespread and spontaneously present. These oscillations are largely organized along the anterior–posterior (AP) axis of the insula. Both the left and right insula showed anterior-­to-posterior decreasing gradients for the power of oscillations in the beta frequency band. The left insula also showed a posterior-to-anterior decreasing frequency gradient and an anterior-to-posterior decreasing power gradient in the theta frequency band. In addition to measuring the power of these oscillations, we also examined the phase of these signals across simultaneous recording channels and found that the insula oscillations in the theta and beta bands are traveling waves. The strength of the traveling waves in each frequency was positively correlated with the amplitude of each oscillation. However, the theta and beta traveling waves were uncoupled to each other in terms of phase and amplitude, which suggested that insular traveling waves in the theta and beta bands operate independently. Our findings provide new insights into the spatiotemporal dynamics and hierarchical organization of neuronal oscillations within the insula, which, given its rich connectivity with widespread cortical regions, indicates that oscillations and traveling waves have an important role in intrainsular and interinsular communications. eLife Sciences Publications, Ltd 2022-05-26 /pmc/articles/PMC9200407/ /pubmed/35616527 http://dx.doi.org/10.7554/eLife.76702 Text en © 2022, Das, Myers et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Neuroscience
Das, Anup
Myers, John
Mathura, Raissa
Shofty, Ben
Metzger, Brian A
Bijanki, Kelly
Wu, Chengyuan
Jacobs, Joshua
Sheth, Sameer A
Spontaneous neuronal oscillations in the human insula are hierarchically organized traveling waves
title Spontaneous neuronal oscillations in the human insula are hierarchically organized traveling waves
title_full Spontaneous neuronal oscillations in the human insula are hierarchically organized traveling waves
title_fullStr Spontaneous neuronal oscillations in the human insula are hierarchically organized traveling waves
title_full_unstemmed Spontaneous neuronal oscillations in the human insula are hierarchically organized traveling waves
title_short Spontaneous neuronal oscillations in the human insula are hierarchically organized traveling waves
title_sort spontaneous neuronal oscillations in the human insula are hierarchically organized traveling waves
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9200407/
https://www.ncbi.nlm.nih.gov/pubmed/35616527
http://dx.doi.org/10.7554/eLife.76702
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