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The left inferior fronto-occipital fasciculus subserves language semantics: a multilevel lesion study

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Abstract

Consequential works in cognitive neuroscience have led to the formulation of an interactive dual-stream model of language processing: the dorsal stream may process the phonological aspects of language, whereas the ventral stream may process the semantic aspects of language. While it is well-accepted that the dorsal route is subserved by the arcuate fasciculus, the structural connectivity of the semantic ventral stream is a matter of dispute. Here we designed a longitudinal study to gain new insights into this central but controversial question. Thirty-one patients harboring a left diffuse low-grade glioma—a rare neurological condition that infiltrates preferentially white matter associative pathways—were assessed with a prototypical task of language (i.e. verbal fluency) before and after surgery. All were operated under local anesthesia with a cortical and subcortical brain mapping—enabling to identify and preserve eloquent structures for language. We performed voxel-based lesion-symptom (VLSM) analyses on pre- and postoperative behavioral data. Preoperatively, we found a significant relationship between semantic fluency scores and the white matter fibers shaping the ventro-lateral connectivity (P < 0.05 corrected). The statistical map was found to substantially overlap with the spatial position of the inferior fronto-occipital fasciculus (IFOF) (37.7 %). Furthermore, a negative correlation was observed between semantic fluency scores and the infiltration volumes in this fasciculus (r = −0.4, P = 0.029). Postoperatively, VLSM analyses were inconclusive. Taken as a whole and when combined with the literature data, our findings strengthen the view that the IFOF plays an essential role in semantic processing and may subserve the direct ventral pathway of language.

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Acknowledgments

G.H. is supported by the Association pour la Recherche sur le Cancer (aides individuelles No. DOC20120605069).

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Authors and Affiliations

  1. Department of Neurosurgery, Hôpital Pasteur, University Hospital Center, 06000, Nice, France

    Fabien Almairac

  2. Department of Neurosurgery, Hôpital Gui de Chauliac, Montpellier University Medical Center, 80 Avenue Augustin Fliche, 34295, Montpellier, France

    Guillaume Herbet, Sylvie Moritz-Gasser & Hugues Duffau

  3. Institute for Neuroscience of Montpellier, INSERM 1051, Team “Plasticity of the Central Nervous System, Stem Cells and Glial Tumors”, Hôpital Saint Eloi, 34091, Montpellier, France

    Guillaume Herbet, Sylvie Moritz-Gasser & Hugues Duffau

  4. University of Montpellier 1, 34967, Montpellier, France

    Guillaume Herbet & Sylvie Moritz-Gasser

  5. Department of Neuroradiology, Hôpital Gui de Chauliac, Montpellier University Medical Center, 34295, Montpellier, France

    Nicolas Menjot de Champfleur

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  1. Fabien Almairac
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  2. Guillaume Herbet
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  3. Sylvie Moritz-Gasser
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  4. Nicolas Menjot de Champfleur
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  5. Hugues Duffau
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Correspondence to Hugues Duffau.

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429_2014_773_MOESM1_ESM.tif

Figure S1. Preoperative voxel-based lesion-symptom mapping (VLSM) analysis for Resid-Sem. MNI coordinates of each section are given, x for axial slices, y for coronal slices, and z for sagittal slices. The map shows only significant voxels with FDR-controlled threshold (P < 0.05 corresponding to Z > 1.99). VLSM analyses performed on Resid-Phono was inconclusive (i.e. no voxels survive the FDR correction) (TIFF 5253 kb)

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Almairac, F., Herbet, G., Moritz-Gasser, S. et al. The left inferior fronto-occipital fasciculus subserves language semantics: a multilevel lesion study. Brain Struct Funct 220, 1983–1995 (2015). https://doi.org/10.1007/s00429-014-0773-1

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  • DOI: https://doi.org/10.1007/s00429-014-0773-1

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