Cargando…

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...

Descripción completa

Detalles Bibliográficos
Autores principales: 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.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
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
_version_ 1785117687651762176
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
work_keys_str_mv AT kocsiszsuzsanna immediateneuralimpactandincompletecompensationaftersemantichubdisconnection
AT jenisonrickl immediateneuralimpactandincompletecompensationaftersemantichubdisconnection
AT taylorpetern immediateneuralimpactandincompletecompensationaftersemantichubdisconnection
AT calmusryanm immediateneuralimpactandincompletecompensationaftersemantichubdisconnection
AT mcmurraybob immediateneuralimpactandincompletecompensationaftersemantichubdisconnection
AT rhonearianee immediateneuralimpactandincompletecompensationaftersemantichubdisconnection
AT sarrettmccalle immediateneuralimpactandincompletecompensationaftersemantichubdisconnection
AT deifeltstreesecarolina immediateneuralimpactandincompletecompensationaftersemantichubdisconnection
AT kikuchiyukiko immediateneuralimpactandincompletecompensationaftersemantichubdisconnection
AT ganderphillipe immediateneuralimpactandincompletecompensationaftersemantichubdisconnection
AT bergerjoeli immediateneuralimpactandincompletecompensationaftersemantichubdisconnection
AT kovachchristopherk immediateneuralimpactandincompletecompensationaftersemantichubdisconnection
AT choiinyong immediateneuralimpactandincompletecompensationaftersemantichubdisconnection
AT greenleejeremyd immediateneuralimpactandincompletecompensationaftersemantichubdisconnection
AT kawasakihiroto immediateneuralimpactandincompletecompensationaftersemantichubdisconnection
AT copethomase immediateneuralimpactandincompletecompensationaftersemantichubdisconnection
AT griffithstimothyd immediateneuralimpactandincompletecompensationaftersemantichubdisconnection
AT howardmatthewa immediateneuralimpactandincompletecompensationaftersemantichubdisconnection
AT petkovchristopheri immediateneuralimpactandincompletecompensationaftersemantichubdisconnection