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Identifying subcortical connectivity during brain tumor surgery: a multimodal study

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Abstract

Bipolar direct electrical stimulation (DES) of an awake patient is the reference technique for identifying brain structures to achieve maximal safe tumor resection. Unfortunately, DES cannot be performed in all cases. Alternative surgical tools are, therefore, needed to aid identification of subcortical connectivity during brain tumor removal. In this pilot study, we sought to (i) evaluate the combined use of evoked potential (EP) and tractography for identification of white matter (WM) tracts under the functional control of DES, and (ii) provide clues to the electrophysiological effects of bipolar stimulation on neural pathways. We included 12 patients (mean age of 38.4 years) who had had a dMRI-based tractography and a functional brain mapping under awake craniotomy for brain tumor removal. Electrophysiological recordings of subcortical evoked potentials (SCEPs) were acquired during bipolar low frequency (2 Hz) stimulation of the WM functional sites identified during brain mapping. SCEPs were successfully triggered in 11 out of 12 patients. The median length of the stimulated fibers was 43.24 ± 19.55 mm, belonging to tracts of median lengths of 89.84 ± 24.65 mm. The electrophysiological (delay, amplitude, and speed of propagation) and structural (number and lengths of streamlines, and mean fractional anisotropy) measures were correlated. In our experimental conditions, SCEPs were essentially limited to a subpart of the bundles, suggesting a selectivity of action of the DES on the brain networks. Correlations between functional, structural, and electrophysiological measures portend the combined use of EPs and tractography as a potential intraoperative tool to achieve maximum safe resection in brain tumor surgery.

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Data availability

The anonymized data acquired during this protocol consisting of preoperative MRIs and intraoperative SCEPs are available upon request to any qualified investigator after completion of a data sharing agreement. The source code for all data processing is freely available at https://doi.org/10.5281/zenodo.6784185.

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Funding

This study was supported and granted by the University Hospital of Nice (grant number: 19-AOIP-01).

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Authors and Affiliations

Authors

Contributions

FA: Conceptualization, Methodology, Validation, Investigation, Resources, Writing—Original Draft, Writing—Review & Editing, Visualization, Supervision, Project administration, Funding acquisition. PI: Methodology, Software, Validation, Investigation, Writing—Original Draft, Writing—Review & Editing, Visualization. MO: Methodology, Investigation, Writing—Original Draft, Visualization. TPo: Methodology, Software, Validation, Investigation, Resources, Data Curation, Writing—Review & Editing. LM: Methodology, Validation, Investigation, Writing—Original Draft, Visualization. SCt: Validation, Investigation, Writing—Original Draft, Visualization. CFz: Investigation, Writing—Original Draft. MCc: Methodology, Software, Validation, Investigation, Resources, Data Curation. RD: Validation, Investigation, Resources, Data Curation, Writing—Review & Editing. DF: Conceptualization, Methodology, Investigation, Resources, Writing—Original Draft, Supervision. PF: Conceptualization, Methodology, Software, Validation, Investigation, Writing—Original Draft, Writing—Review & Editing, Visualization.

Corresponding author

Correspondence to Fabien Almairac.

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Conflict of interests

The authors have no relevant financial or non-financial interests to disclose.

Ethics Approval

This study was approved by a French ethical committee and was registered in the Clinical Trials database (NCT04163315).

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All participating patients have freely given their written informed consent according to the Declaration of Helsinki.

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Almairac, F., Isan, P., Onno, M. et al. Identifying subcortical connectivity during brain tumor surgery: a multimodal study. Brain Struct Funct 228, 815–830 (2023). https://doi.org/10.1007/s00429-023-02623-0

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  • DOI: https://doi.org/10.1007/s00429-023-02623-0

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