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Language reorganization after resection of low-grade gliomas: an fMRI task based connectivity study

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Abstract

Few studies addressed the evolution of brain activity before and after brain tumor resection. Using a fMRI naming task, we evaluated possible underlying plasticity phenomena. Thirty-two patients with left low-grade gliomas (16 women; age = 38.6 ± 8.31 years) and 19 healthy controls (7 women; age = 42.4 ± 12.1) were included in the study. An overt picture-naming task (DO80) was performed pre and post (3 months) surgery, as well as within the MRI in a covert manner. Exams included an injected 3DT1, a T2FLAIR, a DTI and a GE-EPI (task) sequence. Activations maps were compared with picture naming score, FA and MD maps were estimated, a VLSM analysis was performed on tumor masks, and disconnectome maps were reconstructed. Pre-surgery, the left parahippocampal gyrus (LPH) was inversely associated with task performance. Increased pre-post surgery left lingual gyrus (LLG) activity was found related to decreased picture naming performance. The evolution of left lingual gyrus (LLG) activity was negatively associated with the evolution of picture naming performance. In controls, the LPH was functionally connected to the right precentral gyrus (RPCG) and slightly to the LLG. This was not clearly retrieved in the patient group. Preoperatively, the LLG was connected to the left planum temporale and to the right lingual gyrus. The same result was found for controls. Postoperatively, the LLG was only connected to the RPCG. No association was found between evolution of FA/MD and evolution of picture naming performance. There is not one unique pattern of pre- and postoperative plasticity concerning picture-naming performance in DLGG patients.

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Funding

This work was supported by the CHU Montpellier “Appel d’offres internes” and “Programme hospitalier de recherche infirmière et paramédicale” (number ID-RCB 2010-AO1313–36; UF 8674) and LabEx NUMEV project (number AN-10-LABX-20).

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Authors and Affiliations

  1. Department of Neuroradiology, Montpellier University Hospital, Gui de Chauliac Hospital, Montpellier, France

    Jeremy Deverdun, Emmanuelle Le Bars & Nicolas Menjot

  2. I2FH, Institut d’Imagerie Fonctionnelle Humaine, Montpellier University Hospital, Gui de Chauliac Hospital, Montpellier, France

    Jeremy Deverdun, Emmanuelle Le Bars, Nicolas Menjot & Francois Molino

  3. Laboratoire Charles Coulomb, University of Montpellier, 34095, Montpellier, France

    Jeremy Deverdun, Liesjet E. H. van Dokkum, Emmanuelle Le Bars, Nicolas Menjot & Francois Molino

  4. Department of Neurosurgery, Montpellier University Hospital Center, Gui de Chauliac Hospital, Montpellier, France

    Guillaume Herbet, Hugues Duffau & Sylvie Moritz Gasser

  5. Team “Plasticity of Central Nervous System, Stem Cells and Glial Tumors”, INSERM U1051, Institute of Neurosciences of Montpellier, Montpellier, France

    Guillaume Herbet, Hugues Duffau & Sylvie Moritz Gasser

  6. Epidemiology Department, University Hospital, Clinical Investigation Center, Inserm-CIC, 1411, Montpellier, France

    Thibault Mura, Benedicte D’agata & Marie-Christine Picot

  7. Department of Speech-Language Therapy, University of Medicine, Montpellier, France

    Sylvie Moritz Gasser

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  1. Jeremy Deverdun
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Correspondence to Jeremy Deverdun.

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Ethical committee of Montpellier gave its approval for this work and procedures were compliant with the declaration of Helsinki. Informed consent was obtained from all individual participants. Authors report no potential conflicts of interest.

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Glossary

DLGG

Diffuse low grade glioma

FA

Fractional anisotropy

FDR

False discovery rate

FMRI

Functional Magnetic Resonance Imaging

FWE

Family wise error

IFOF

Inferior Fronto-Occipital Fasciculus

ILF

Inferior Longitudinal Fasciculus

ITG

Inferior Temporal Gyrus

LLG

left lingual gyrus

LPH

Left parahippocampus

MD

Mean diffusivity

ROI

Region of interest

RPCG

Right precentral gyrus

VLSM

Voxel-based lesion-symptom mapping

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Deverdun, J., van Dokkum, L.E.H., Le Bars, E. et al. Language reorganization after resection of low-grade gliomas: an fMRI task based connectivity study. Brain Imaging and Behavior 14, 1779–1791 (2020). https://doi.org/10.1007/s11682-019-00114-7

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