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Immediate neural impact and incomplete compensation after semantic hub disconnection
The human brain extracts meaning using an extensive neural system for semantic knowledge. Whether broadly distributed systems depend on or can compensate after losing a highly interconnected hub is controversial. We report intracranial recordings from two patients during a speech prediction task, ob...
Autores principales: | , , , , , , , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Nature Publishing Group UK
2023
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10560235/ https://www.ncbi.nlm.nih.gov/pubmed/37805497 http://dx.doi.org/10.1038/s41467-023-42088-7 |
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author | Kocsis, Zsuzsanna Jenison, Rick L. Taylor, Peter N. Calmus, Ryan M. McMurray, Bob Rhone, Ariane E. Sarrett, McCall E. Deifelt Streese, Carolina Kikuchi, Yukiko Gander, Phillip E. Berger, Joel I. Kovach, Christopher K. Choi, Inyong Greenlee, Jeremy D. Kawasaki, Hiroto Cope, Thomas E. Griffiths, Timothy D. Howard, Matthew A. Petkov, Christopher I. |
author_facet | Kocsis, Zsuzsanna Jenison, Rick L. Taylor, Peter N. Calmus, Ryan M. McMurray, Bob Rhone, Ariane E. Sarrett, McCall E. Deifelt Streese, Carolina Kikuchi, Yukiko Gander, Phillip E. Berger, Joel I. Kovach, Christopher K. Choi, Inyong Greenlee, Jeremy D. Kawasaki, Hiroto Cope, Thomas E. Griffiths, Timothy D. Howard, Matthew A. Petkov, Christopher I. |
author_sort | Kocsis, Zsuzsanna |
collection | PubMed |
description | The human brain extracts meaning using an extensive neural system for semantic knowledge. Whether broadly distributed systems depend on or can compensate after losing a highly interconnected hub is controversial. We report intracranial recordings from two patients during a speech prediction task, obtained minutes before and after neurosurgical treatment requiring disconnection of the left anterior temporal lobe (ATL), a candidate semantic knowledge hub. Informed by modern diaschisis and predictive coding frameworks, we tested hypotheses ranging from solely neural network disruption to complete compensation by the indirectly affected language-related and speech-processing sites. Immediately after ATL disconnection, we observed neurophysiological alterations in the recorded frontal and auditory sites, providing direct evidence for the importance of the ATL as a semantic hub. We also obtained evidence for rapid, albeit incomplete, attempts at neural network compensation, with neural impact largely in the forms stipulated by the predictive coding framework, in specificity, and the modern diaschisis framework, more generally. The overall results validate these frameworks and reveal an immediate impact and capability of the human brain to adjust after losing a brain hub. |
format | Online Article Text |
id | pubmed-10560235 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | Nature Publishing Group UK |
record_format | MEDLINE/PubMed |
spelling | pubmed-105602352023-10-09 Immediate neural impact and incomplete compensation after semantic hub disconnection Kocsis, Zsuzsanna Jenison, Rick L. Taylor, Peter N. Calmus, Ryan M. McMurray, Bob Rhone, Ariane E. Sarrett, McCall E. Deifelt Streese, Carolina Kikuchi, Yukiko Gander, Phillip E. Berger, Joel I. Kovach, Christopher K. Choi, Inyong Greenlee, Jeremy D. Kawasaki, Hiroto Cope, Thomas E. Griffiths, Timothy D. Howard, Matthew A. Petkov, Christopher I. Nat Commun Article The human brain extracts meaning using an extensive neural system for semantic knowledge. Whether broadly distributed systems depend on or can compensate after losing a highly interconnected hub is controversial. We report intracranial recordings from two patients during a speech prediction task, obtained minutes before and after neurosurgical treatment requiring disconnection of the left anterior temporal lobe (ATL), a candidate semantic knowledge hub. Informed by modern diaschisis and predictive coding frameworks, we tested hypotheses ranging from solely neural network disruption to complete compensation by the indirectly affected language-related and speech-processing sites. Immediately after ATL disconnection, we observed neurophysiological alterations in the recorded frontal and auditory sites, providing direct evidence for the importance of the ATL as a semantic hub. We also obtained evidence for rapid, albeit incomplete, attempts at neural network compensation, with neural impact largely in the forms stipulated by the predictive coding framework, in specificity, and the modern diaschisis framework, more generally. The overall results validate these frameworks and reveal an immediate impact and capability of the human brain to adjust after losing a brain hub. Nature Publishing Group UK 2023-10-07 /pmc/articles/PMC10560235/ /pubmed/37805497 http://dx.doi.org/10.1038/s41467-023-42088-7 Text en © The Author(s) 2023, corrected publication 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Article Kocsis, Zsuzsanna Jenison, Rick L. Taylor, Peter N. Calmus, Ryan M. McMurray, Bob Rhone, Ariane E. Sarrett, McCall E. Deifelt Streese, Carolina Kikuchi, Yukiko Gander, Phillip E. Berger, Joel I. Kovach, Christopher K. Choi, Inyong Greenlee, Jeremy D. Kawasaki, Hiroto Cope, Thomas E. Griffiths, Timothy D. Howard, Matthew A. Petkov, Christopher I. Immediate neural impact and incomplete compensation after semantic hub disconnection |
title | Immediate neural impact and incomplete compensation after semantic hub disconnection |
title_full | Immediate neural impact and incomplete compensation after semantic hub disconnection |
title_fullStr | Immediate neural impact and incomplete compensation after semantic hub disconnection |
title_full_unstemmed | Immediate neural impact and incomplete compensation after semantic hub disconnection |
title_short | Immediate neural impact and incomplete compensation after semantic hub disconnection |
title_sort | immediate neural impact and incomplete compensation after semantic hub disconnection |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10560235/ https://www.ncbi.nlm.nih.gov/pubmed/37805497 http://dx.doi.org/10.1038/s41467-023-42088-7 |
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