Predicting attention deficits and functional recovery after glioma resection through functional executive networks: insights from dynamic properties

Abstract

Background: Postoperative short-term attentional and executive dysfunctions are common after brain tumor resection, significantly impacting patients' quality of life and functional recovery. The current study investigated whether presurgical functional dynamics of key brain networks supporting executive functioning could predict postoperative neuropsychological outcomes. Methods: Twenty-two patients with gliomas underwent longitudinal resting-state fMRI scans (before and three-months after surgery), along with neuropsychological assessments (before, one-week and three-months after surgery). Co-activation patterns analysis (CAPs) characterized the functional dynamic properties of executive networks, including the Fronto-parietal (FPN) and Dorsal Attention networks (DAN). Temporal network properties were examined for stability, integration, and centrality over timepoints. Partial least squares analyses and linear models explored associations between network dynamics and cognitive functioning. Results: Immediate post-surgical attentional deficits were linked to pre-surgical FPN properties revealing associated dynamic patterns of network activation. Pre-surgical FPN temporal properties predicted not only immediate appearance or persistence of post-resection deficits, but also the longitudinal progression of attentional performance otherwise neglected. However, regardless of the severity of attentional deficit, at three months post-surgery, temporal properties and neuropsychological profiles did not significantly differ from the pre-surgical ones, indicating recovery to baseline beyond treatment strategies. Conclusions: Our study demonstrates that presurgical dynamic properties of intrinsic executive networks alone can predict short-term postoperative neuropsychological outcomes, highlighting the clinical utility of temporal functional connectivity. These findings emphasize the potential for using intrinsic brain activity dynamics as predictive markers for postoperative recovery and planning tailored rehabilitation interventions for cognitive deficits.

Competing Interest Statement

The authors have declared no competing interest.

Funding Statement

Autonomous Province of Trento, Italy: Project: NeuSurPlan and integrated approach to neurosurgery planning based on multimodal data to S.S. and J.J. Italian Ministry of Education, University and Research: Dipartimento di Eccellenza project 2018-2022 to F.S. Lucarelli Irion Foundation, Rovereto, Italy, who supported F.S.

Author Declarations

I confirm all relevant ethical guidelines have been followed, and any necessary IRB and/or ethics committee approvals have been obtained.

Yes

The details of the IRB/oversight body that provided approval or exemption for the research described are given below:

Approval for this study was obtained by the Ethical Committee of the Azienda Provinciale per i Servizi Sanitari (APSS, Neusurplan project, authorization ID A734).

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Yes

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I have followed all appropriate research reporting guidelines, such as any relevant EQUATOR Network research reporting checklist(s) and other pertinent material, if applicable.

Yes

Data Availability

Data will be made available in de-identified format upon request to the authors.

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