Tumour-infiltrated cortex participates in large-scale cognitive circuits

Ayan S. Mandal, Chemda Wiener, Moataz Assem, Rafael Romero-Garcia, Pedro Coelho, Alexa McDonald, Emma Woodberry, Robert C. Morris, Stephen J. Price, John Duncan, Thomas Santarius, John Suckling, Michael G. Hart, Yaara Erez

Research output: Contribution to journalArticlepeer-review

1 Scopus citations

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.

Original languageEnglish
Pages (from-to)1-15
Number of pages15
JournalCortex
Volume173
DOIs
StatePublished - Apr 2024

Bibliographical note

Publisher Copyright:
© 2024 The Authors

Funding

The Gates Cambridge Trust provided financial support in the form of a Gates Cambridge Scholarship to ASM (OPP1144). The Royal Society provided financial support in the form of a Royal Society Dorothy Hodgkin Research Fellowship to YE (DH130100). The Applebaum Foundation provided financial support in the form of a grant award to YE. Cambridge Commonwealth European and International Trust provided financial support in the form of a Yousef Jameel scholarship to MA. Guarantors of Brain provided financial support in the form of a Post-Doctoral Fellowship award to RRG. The National Institute for Health Research (NIHR, UK) provided financial support in the form of a Clinician Scientist Award 35 to SJP (ref: NIHR/CS/009/011). The Brain Tumour Charity provided financial support in the form of a grant award to MGH, YE and TS (ref: RG86218). JD was funded by a Medical Research Council grant (SUAG/045.G101400). The Gates Cambridge Trust provided financial support in the form of a Gates Cambridge Scholarship to ASM ( OPP1144 ). The Royal Society provided financial support in the form of a Royal Society Dorothy Hodgkin Research Fellowship to YE ( DH130100 ). The Applebaum Foundation provided financial support in the form of a grant award to YE. Cambridge Commonwealth European and International Trust provided financial support in the form of a Yousef Jameel scholarship to MA. Guarantors of Brain provided financial support in the form of a Post-Doctoral Fellowship award to RRG. The National Institute for Health Research (NIHR, UK) provided financial support in the form of a Clinician Scientist Award 35 to SJP (ref: NIHR/CS/009/011). The Brain Tumour Charity provided financial support in the form of a grant award to MGH, YE and TS (ref: RG86218). JD was funded by a Medical Research Council grant ( SUAG/045.G101400 ).

FundersFunder number
International Trust
Applebaum Foundation
Medical Research CouncilSUAG/045, G101400
National Institute for Health and Care ResearchNIHR/CS/009/011
Royal SocietyDH130100
Brain Tumour CharityRG86218
Gates Cambridge TrustOPP1144

    Keywords

    • Brain tumour
    • Electrocorticography (ECOG)
    • Executive function
    • Functional connectivity
    • Glioma
    • Neural circuits
    • fMRI

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