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Tumour-infiltrated cortex participates in large-scale cognitive circuits.

Mandal, AS; Wiener, C; Assem, M; Romero-Garcia, R; Coelho, P; McDonald, A; Woodberry, E; Morris, RC; Price, SJ; Duncan, J; et al. Mandal, AS; Wiener, C; Assem, M; Romero-Garcia, R; Coelho, P; McDonald, A; Woodberry, E; Morris, RC; Price, SJ; Duncan, J; Santarius, T; Suckling, J; Hart, MG; Erez, Y (2024) Tumour-infiltrated cortex participates in large-scale cognitive circuits. Cortex, 173. pp. 1-15. ISSN 1973-8102 https://doi.org/10.1016/j.cortex.2024.01.004
SGUL Authors: Hart, Michael Gavin

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Abstract

The extent to which tumour-infiltrated brain tissue contributes to cognitive function remains unclear. We tested the hypothesis that cortical tissue infiltrated by diffuse gliomas participates in large-scale cognitive circuits using a unique combination of intracranial electrocorticography (ECoG) and resting-state functional magnetic resonance (fMRI) imaging in four patients. We also assessed the relationship between functional connectivity with tumour-infiltrated tissue and long-term cognitive outcomes in a larger, overlapping cohort of 17 patients. We observed significant task-related high gamma (70-250 Hz) power modulations in tumour-infiltrated cortex in response to increased cognitive effort (i.e., switch counting compared to simple counting), implying preserved functionality of neoplastic tissue for complex tasks probing executive function. We found that tumour locations corresponding to task-responsive electrodes exhibited functional connectivity patterns that significantly co-localised with canonical brain networks implicated in executive function. Specifically, we discovered that tumour-infiltrated cortex with larger task-related high gamma power modulations tended to be more functionally connected to the dorsal attention network (DAN). Finally, we demonstrated that tumour-DAN connectivity is evident across a larger cohort of patients with gliomas and that it relates to long-term postsurgical outcomes in goal-directed attention. Overall, this study contributes convergent fMRI-ECoG evidence that tumour-infiltrated cortex participates in large-scale neurocognitive circuits that support executive function in health. These findings underscore the potential clinical utility of mapping large-scale connectivity of tumour-infiltrated tissue in the care of patients with diffuse gliomas.

Item Type: Article
Additional Information: © 2024 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
Keywords: Brain tumour, Electrocorticography (ECOG), Executive function, Functional connectivity, Glioma, Neural circuits, fMRI, 1109 Neurosciences, 1701 Psychology, 1702 Cognitive Sciences, Experimental Psychology
Journal or Publication Title: Cortex
ISSN: 1973-8102
Language: eng
Dates:
DateEvent
13 February 2024Published
30 January 2024Published Online
11 January 2024Accepted
Publisher License: Creative Commons: Attribution 4.0
Projects:
Project IDFunderFunder ID
OPP1144Gates Cambridge Trusthttp://dx.doi.org/10.13039/501100005370
DH130100Royal Societyhttp://dx.doi.org/10.13039/501100000288
UNSPECIFIEDCambridge Commonwealth European and International TrustUNSPECIFIED
UNSPECIFIEDGuarantors of Brainhttp://dx.doi.org/10.13039/501100000627
NIHR/CS/009/011National Institute for Health Researchhttp://dx.doi.org/10.13039/501100000272
RG86218Brain Tumour Charityhttp://dx.doi.org/10.13039/501100002203
SUAG/045.G101400Medical Research Councilhttp://dx.doi.org/10.13039/501100000265
PubMed ID: 38354669
Go to PubMed abstract
URI: https://openaccess.sgul.ac.uk/id/eprint/116289
Publisher's version: https://doi.org/10.1016/j.cortex.2024.01.004

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