Dissociating motor–speech from lexico-semantic systems in the left frontal lobe: insight from a series of 17 awake intraoperative mappings in glioma patients
Brain Struct Funct. 2019-01-14; 224(3): 1151-1165
DOI: 10.1007/s00429-019-01827-7
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Corrivetti F(1), de Schotten MT(2), Poisson I(1), Froelich S(1)(3), Descoteaux M(4), Rheault F(1)(4), Mandonnet E(5)(6)(7).
Author information:
(1)Department of Neurosurgery, Lariboisière Hospital, APHP, 2 rue Ambroise Paré,
75010, Paris, France.
(2)Brain connectivity and behaviour group, Frontlab, Inserm, CNRS, institut du
cerveau et la moelle (ICM), hôpital Pitié-Salpêtrière, UPMC université Paris 06,
Sorbonne universités, 75013, Paris, France.
(3)University Paris 7, Paris, France.
(4)Sherbrooke Connectivity Imaging Lab (SCIL), Computer Science Department,
Université de Sherbrooke, Sherbrooke, Canada.
(5)Department of Neurosurgery, Lariboisière Hospital, APHP, 2 rue Ambroise Paré,
75010, Paris, France. .
(6)Brain connectivity and behaviour group, Frontlab, Inserm, CNRS, institut du
cerveau et la moelle (ICM), hôpital Pitié-Salpêtrière, UPMC université Paris 06,
Sorbonne universités, 75013, Paris, France. .
(7)University Paris 7, Paris, France. .
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.