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Immediate neural impact and incomplete compensation after semantic hub disconnection

Lookup NU author(s): Dr Ryan Calmus, Dr Yuki Kikuchi, Professor Tim GriffithsORCiD, Professor Christopher Petkov

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This work is licensed under a Creative Commons Attribution 4.0 International License (CC BY 4.0).


Abstract

© 2023, Springer Nature Limited.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.


Publication metadata

Author(s): Kocsis Z, Jenison RL, Taylor PN, Calmus RM, McMurray B, Rhone AE, Sarrett MCE, Deifelt Streese C, Kikuchi Y, Gander PE, Berger JI, Kovach CK, Choi I, Greenlee JD, Kawasaki H, Cope TE, Griffiths TD, Howard MA, Petkov CI

Publication type: Article

Publication status: Published

Journal: Nature Communications

Year: 2023

Volume: 14

Issue: 1

Online publication date: 07/10/2023

Acceptance date: 28/09/2023

Date deposited: 01/11/2023

ISSN (electronic): 2041-1723

Publisher: Nature Research

URL: https://doi.org/10.1038/s41467-023-42088-7

DOI: 10.1038/s41467-023-42088-7

Data Access Statement: The datasets generated in this study have been deposited in the Zenodo database under accession code https://doi.org/10.5281/zenodo.8110724. Source data is provided with this paper. Source data are provided with this paper. Code availability No custom software was used during the current study. Analysis scripts are available from the corresponding authors upon request.

PubMed id: 37805497


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Funding

Funder referenceFunder name
CIP: ERC CoG
European Research Council
MECHIDENT
MAH: R01–DC04290
National Institutes of Health USA
U01-NP103780
Wellcome Trust
WT091681MA
WT092606AIA

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