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Comparison between inferior frontal gyrus intrinsic connectivity network and verb-generation task fMRI network for presurgical language mapping in healthy controls and in glioma patients

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Abstract

Task-based functional MRI (tb-fMRI) represents an extremely valuable approach for the identification of language eloquent regions for presurgical mapping in patients with brain tumors. However, its routinely application is limited by patient-related factors, such as cognitive disability and difficulty in coping with long-time acquisitions, and by technical factors, such as lack of equipment availability for stimuli delivery. Resting-state fMRI (rs-fMRI) instead, allows the identification of distinct language networks in a 10-min acquisition without the need of performing active tasks and using specific equipment. Therefore, to test the feasibility of rs-fMRI as a preoperative mapping tool, we reconstructed a lexico-semantic intrinsic connectivity network (ICN) in healthy controls (HC) and in a case series of patients with gliomas and compared the organization of this language network with the one derived from tb-fMRI in the patient’s group. We studied three patients with extra-frontal gliomas who underwent functional mapping with auditory verb-generation (AVG) task and rs-fMRI with a seed in the left inferior frontal gyrus (IFG). First, we identified the functional connected areas to the IFG in HC. We qualitatively compared these areas with those that showed functional activation in AVG task derived from Neurosynth meta-analysis. Last, in each patient we performed single-subject analyses both for rs- and tb-fMRI, and we evaluated the spatial overlap between the two approaches. In HC, the IFG-ICN network showed a predominant left fronto-temporal functional connectivity in regions overlapping with the AVG network derived from a meta-analysis. In two patients, rs- and tb-fMRI showed comparable patterns of activation in left fronto-temporal regions, with different levels of contralateral activations. The third patient could not accomplish the AVG task and thus it was not possible to make any comparison with the ICN. However, in this patient, task-free approach disclosed a consistent network of fronto-temporal regions as in HC, and additional parietal regions. Our preliminary findings support the value of rs-fMRI approach for presurgical mapping, particularly for identifying left fronto-temporal core language-related areas in glioma patients. In a preoperative setting, rs-fMRI approach could represent a powerful tool for the identification of eloquent language areas, especially in patients with language or cognitive impairments.

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Data availability

The datasets of this study is available from the authors upon request.

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The submitted work has not been published previously and is not being considered for publication elsewhere.

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The authors did not receive support from any organization for the submitted work.

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Authors and Affiliations

Authors

Contributions

SC: data acquisition and analysis, study design and data interpretation. GB: data analysis, study design and data interpretation. AC: data acquisition, study design and data interpretation. FS: data analysis and interpretation. AI: data acquisition. MB, RLB, SA, PM: collection of clinical/neurosurgical data, data interpretation. MLGT, MLM, AF: conception and study design, data interpretation.

Corresponding author

Correspondence to Antonella Castellano.

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All procedures performed involving human participants were reviewed and approved by Local ethical committee of Ospedale San Raffaele, Milan, Italy.

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All subjects provided signed informed consent prior to MR imaging.

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None of the authors have a conflict of interest to declare.

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Sara Cirillo and Giovanni Battistella share first authorship.

Andrea Falini and Maria Luisa Mandelli share last authorship.

Supplementary Information

ESM 1

Fig. 1 (a, b, c, d, e) Axial slices of subject-level rs-fMRI ICN of the triIFG on the left (p <0.05; r  ≥ 0.3) and auditory verb-generation tb-fMRI in the five selected cases on the right (p <0.05 FWE corrected, cluster extent >30 voxels). *fig.1, d - Auditory verb-generation tb-fMRI for Case #3 was shown using an uncorrected threshold (p<0.001, uncorrected, cluster extent k >10). (PNG 1973 kb)

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ESM 2

Fig. 2 Left hemisphere overlap (yellow color) between IFG-ICN (red color) and AVG tb-fMRI (green) networks in Case #1 (a), Case #2 (b), Case #4 (c) and Case #5 (d) superimposed on a template. (PNG 857 kb)

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Cirillo, S., Battistella, G., Castellano, A. et al. Comparison between inferior frontal gyrus intrinsic connectivity network and verb-generation task fMRI network for presurgical language mapping in healthy controls and in glioma patients. Brain Imaging and Behavior 16, 2569–2585 (2022). https://doi.org/10.1007/s11682-022-00712-y

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