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Dissociating motor–speech from lexico-semantic systems in the left frontal lobe: insight from a series of 17 awake intraoperative mappings in glioma patients

  • Francesco Corrivetti
  • Michel Thiebaut de Schotten
  • Isabelle Poisson
  • Sébastien Froelich
  • Maxime Descoteaux
  • François Rheault
  • Emmanuel MandonnetEmail author
Original Article
  • 36 Downloads

Abstract

Functional brain mapping during awake surgery procedures is the gold standard technique in the management of left frontal lobe tumors. Nevertheless, a unified picture of the language subsystems encountered during left frontal lobe mapping is still lacking. We retrospectively analyzed the 49 cortical and the 33 axonal sites of functional language mapping performed in 17 patients operated for a left frontal lobe glioma under awake conditions. Sites were tagged on the postoperative MRI, based on anatomical landmarks and intraoperative photography. All MRIs and tags were then registered in the MNI template. Speech disturbances related to motor functions (speech arrest—with or without superior limb arrest—, stuttering, and vocalization) were grouped together as “motor–speech” responses. Anomias, semantic paraphasia, perseverations, and PPTT errors were classified as “lexico-semantic” responses. MNI-registered axonal sites were used as seed for computing disconnectome maps from a tractogram atlas of ten healthy individuals, as implemented in the BCB toolkit. The cortical distribution of lexico-semantic responses appeared to be located anteriorly (pars triangularis of the inferior frontal gyrus and posterior end of the middle and superior frontal gyrus) compared to motor–speech responses (lower end of the precentral gyrus and pars opercularis). Within the white matter, motor–speech responses and lexico-semantic responses overlapped on the trajectory of the aslant and fronto-striatal tracts, but the lexico-semantic sites were located more anteriorly (mean Y coordinate on the MNI system was 21.2 mm for lexico-semantic sites and 14.3 mm for the motor–speech sites; Wilcoxon test: W = 60.5, p = 0.03). Moreover, disconnectome maps evidenced a clear distinction between the two subsystems: posterior fronto-striatal and frontal aslant tracts, corpus callosum and cortico-spinal tract were related to the motor–speech sites, whereas anterior frontal aslant tract, inferior-fronto-occipital fasciculus (IFOF) and anterior thalamic radiations were related to the lexico-semantic sites. Hence, we evidenced distinct anatomical substrates for the motor–speech and lexico-semantic systems. Regarding the aslant/fronto-striatal system, an anterior to posterior gradient was found, with a lexico-semantic role for the anterior part and a motor–speech involvement for the posterior part. For tumors abutting the precentral sulcus, posterior boundaries of the resection are made of motor–speech sites, meaning that the anteriorly located lexico-semantic system is no more functional, as a result of network reorganization by plasticity.

Keywords

Awake surgery Intraoperative brain mapping Frontal lobe Electrical stimulation Lexico-semantic system Speech 

Abbreviations

DEBS

Direct electrical brain stimulation

SFG

Superior frontal gyrus

MFG

Middle frontal gyrus

IFG

Inferior frontal gyrus

FAT

Frontal aslant tract

FST

Fronto-striatal tract

fMRI

Functional magnetic resonance imaging

MRI

Magnetic resonance imaging

Pop

Pars opercularis

Ptr

Pars triangularis

SMA

Supplementary motor area

vPMC

Ventral pre-motor cortex

IFOF

Inferior fronto-occipital fasciculus

Notes

Acknowledgements

MTdS received fundings from the “Agence Nationale de la Recherche” [grants number ANR-13-JSV4-0001-01] and from the Fondation pour la Recherche Médicale (FRM), as well as from the program “Investissements d’avenir” ANR-10-IAIHU-06. EM received funding from the AP-HP (Contrat de Recherche Clinique, CRC chirurgie 2016) and INSERM (Contrat Interface 2018).

Compliance with ethical standards

Conflict of interest

The authors have no conflict of interest to declare.

Ethical approval

The study was approved by the local ethics committee of Pôle Neurosciences of Lariboisière Hospital. This study complied with the ethical standards.

Informed consent

All patients gave signed consent for the retrospective use of clinical and radiological data.

Supplementary material

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Supplementary material 4 (XLS 101 KB)

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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Francesco Corrivetti
    • 1
  • Michel Thiebaut de Schotten
    • 2
  • Isabelle Poisson
    • 1
  • Sébastien Froelich
    • 1
    • 3
  • Maxime Descoteaux
    • 4
  • François Rheault
    • 1
    • 4
  • Emmanuel Mandonnet
    • 1
    • 2
    • 3
    Email author return OK on get
  1. 1.Department of NeurosurgeryLariboisière Hospital, APHPParisFrance
  2. 2.Brain connectivity and behaviour group, FrontlabInserm, CNRS, institut du cerveau et la moelle (ICM), hôpital Pitié-Salpêtrière, UPMC université Paris 06, Sorbonne universitésParisFrance
  3. 3.University Paris 7ParisFrance
  4. 4.Sherbrooke Connectivity Imaging Lab (SCIL), Computer Science DepartmentUniversité de SherbrookeSherbrookeCanada

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