Intraoperative subcortical stimulation mapping of language pathways in a consecutive series of 115 patients with Grade II glioma in the left dominant hemisphere

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Object

Despite better knowledge of cortical language organization, its subcortical anatomofunctional connectivity remains poorly understood. The authors used intraoperative subcortical stimulation in awake patients undergoing operation for a glioma in the left dominant hemisphere to map the language pathways and to determine the contribution of such a method to surgical results.

Methods

One hundred fifteen patients harboring a World Health Organization Grade II glioma within language areas underwent operation after induction of local anesthesia, using direct electrical stimulation to perform online cortical and subcortical language mapping throughout the resection.

Results

After detection of cortical language sites, the authors identified 1 or several of the following subcortical language pathways in all patients: 1) arcuate fasciculus, eliciting phonemic paraphasia when stimulated; 2) inferior frontooccipital fasciculus, generating semantic paraphasia when stimulated; 3) subcallosal fasciculus, inducing transcortical motor aphasia during stimulation; 4) frontoparietal phonological loop, eliciting speech apraxia during stimulation; and 5) fibers coming from the ventral premotor cortex, inducing anarthria when stimulated. These structures were preserved, representing the limits of the resection. Despite a transient immediate postoperative worsening, all but 2 patients (98%) returned to baseline or better. On control MR imaging, 83% of resections were total or subtotal.

Conclusions

These results represent the largest experience with human subcortical language mapping ever reported. The use of intraoperative cortical and subcortical stimulation gives a unique opportunity to perform an accurate and reliable real-time anatomofunctional study of language connectivity. Such knowledge of the individual organization of language networks enables practitioners to optimize the benefit-to-risk ratio of surgery for Grade II glioma within the left dominant hemisphere.

Abbreviations used in this paper: BDAE = Boston Diagnostic Aphasia Examination; DT = diffusion tensor; fMR = functional MR; KPS = Karnofsky Performance Scale; WHO = World Health Organization.

Article Information

Address correspondence to: Hugues Duffau, M.D., Ph.D., Department of Neurosurgery, Hôpital Gui de Chauliac, CHU Montpellier, 80 Av Augustin Fliche, 34295 Montpellier, France. email: h-duffau@chu-montpellier.fr.

© AANS, except where prohibited by US copyright law.

Headings

Figures

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    Arcuate fasciculus: images showing the dorsal phonological stream. a: Cadaveric specimen showing the anatomical trajectory of the white matter of the superior longitudinal fasciculus (slf). (Adapted with permission from Türe U, Yaşargil DCH, Al-Mefty O, Yaşargil MG: Topographic anatomy of the insular region. J Neurosurg 90:720–733, 1999.) b–e: Intraoperative photographs and corresponding postoperative MR images showing the surgical field in different patients who underwent surgery for a WHO Grade II glioma in various brain locations (b, temporal; c, parietal; d, insular; e, frontal). (Adapted from Duffau H, Capelle L, Sichez N, Denvil D, Lopes M, Sichez JP, et al: Intraoperative mapping of the subcortical language pathways using direct stimulations. An anatomo-functional study. Brain 125:199–214, 2002. Reprinted by permission of Oxford University Press.) In all cases, the deep functional boundary of the resection was given by a part of the arcuate fasciculus, identified by subcortical mapping. Electrical stimulation of this tract systematically induced phonemic paraphasia. The precise locations where these language disorders have been induced were marked intraoperatively by numbered tags in the depth of the cavity. These sites are shown by the arrows on the postoperative anatomical imaging.

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    Inferior frontooccipital fasciculus: images showing the ventral semantic stream. a: Cadaveric specimen showing the anatomical trajectory of the white matter bundle of the inferior frontooccipital fasciculus (of). (Adapted with permission from Türe U, Yaşargil DCH, Al-Mefty O, Yaşargil MG: Topographic anatomy of the insular region. J Neurosurg 90:720–733, 1999.) b–d: Intraoperative photographs and corresponding postoperative images showing the surgical field in different patients who underwent surgery for a WHO Grade II glioma in various brain locations (b, temporal; c, insular; d, frontal). (Adapted from Duffau H, Gatignol P, Mandonnet E, Peruzzi P, Tzourio-Mazoyer N, Capelle L: New insights into the anatomo-functional connectivity of the semantic system: a study using corticosubcortical electrostimulations. Brain 128:797–810, 2005. Reprinted by permission of the authors.) In all cases, the deep functional boundary of the resection was given by a part of the inferior frontooccipital fasciculus, identified by subcortical mapping. Electrical stimulation of this tract systematically induced semantic paraphasia. The precise locations where these language disorders have been induced were marked intraoperatively by numbered tags in the depth of the cavity. These sites are shown by the arrows on the postoperative anatomical imaging. c = claustrum.

  • View in gallery

    Left: Intraoperative photograph after resection of a WHO Grade II glioma involving the left middle gyrus. The subcortical tags correspond to the following language pathways: star (mesial boundary), subcallosal fasciculus (inducing transcortical motor aphasia during stimulation); 24 (posterolateral boundary), fibers coming from the ventral premotor cortex (cortical tags 17 and 18), eliciting anarthria when stimulated; 26 (anterolateral boundary), inferior frontooccipital fasciculus, eliciting semantic paraphasia during stimulation. Right: Immediate postoperative axial and coronal T1-weighted enhanced MR images. The straight arrows show the mesial wall of the cavity, corresponding to the subcallosal fasciculus. The curved arrows show the posterolateral wall of the cavity, corresponding to the fibers coming from the ventral premotor cortex, and which run to the periventricular white matter. A = anterior; P = posterior.

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    Left: Intraoperative photograph obtained after resection of a WHO Grade II glioma involving the left retrocentral gyrus and supramarginal gyrus. The subcortical tags correspond to the frontoparietal phonological loop, eliciting articulatory disorders during stimulation (tags 25, 27, and 23). Right: Immediate postoperative axial T1-weighted enhanced MR image. The arrow shows the deep wall of the cavity, corresponding to the frontoparietal phonological loop, that is, to the lateral part of the superior longitudinal fasciculus.

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