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Extended Broca’s Area in the Functional Connectome of Language in Adults: Combined Cortical and Subcortical Single-Subject Analysis Using fMRI and DTI Tractography

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Abstract

Traditional models of the human language circuitry encompass three cortical areas, Broca’s, Geschwind’s and Wernicke’s, and their connectivity through white matter fascicles. The neural connectivity deep to these cortical areas remains poorly understood, as does the macroscopic functional organization of the cortico-subcortical language circuitry. In an effort to expand current knowledge, we combined functional MRI (fMRI) and diffusion tensor imaging to explore subject-specific structural and functional macroscopic connectivity, focusing on Broca’s area. Fascicles were studied using diffusion tensor imaging fiber tracking seeded from volumes placed manually within the white matter. White matter fascicles and fMRI-derived clusters (antonym-generation task) of positive and negative blood-oxygen-level-dependent (BOLD) signal were co-registered with 3-D renderings of the brain in 12 healthy subjects. Fascicles connecting BOLD-derived clusters were analyzed within specific cortical areas: Broca’s, with the pars triangularis, the pars opercularis, and the pars orbitaris; Geschwind’s and Wernicke’s; the premotor cortex, the dorsal supplementary motor area, the middle temporal gyrus, the dorsal prefrontal cortex and the frontopolar region. We found a functional connectome divisible into three systems—anterior, superior and inferior—around the insula, more complex than previously thought, particularly with respect to a new extended Broca’s area. The extended Broca’s area involves two new fascicles: the operculo-premotor fascicle comprised of well-organized U-shaped fibers that connect the pars opercularis with the premotor region; and (2) the triangulo-orbitaris system comprised of intermingled U-shaped fibers that connect the pars triangularis with the pars orbitaris. The findings enhance our understanding of language function.

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Acknowledgments

We thank Wentao Wu, Isaiah Norton, Wendy Plesniak, and Nicole Aucoin for their technical support. We thank Ann Adams for her editorial advice. We are grateful to the community and major sponsors and contributors to Slicer (http://www.slicer.org/pages/Acknowledgments) who permitted us to use the most recent technologies of real-time fiber tracking. This work is part of the National Alliance for Medical Image Computing (NA-MIC), funded by the National Institutes of Health through the NIH Roadmap for Medical Research, Grant U54 EB005149. Information on the National Centers for Biomedical Computing can be obtained from http://nihroadmap.nih.gov/bioinformatics. This work was also supported in part by NIH grants U41-RR019703, P41-RR13218, and P01 CA067165 and by the ITMO Health Technologies (Institut Thématique Multi-Organismes Technologies pour la Santé).

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Correspondence to Jean-Jacques Lemaire.

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Lemaire, JJ., Golby, A., Wells, W.M. et al. Extended Broca’s Area in the Functional Connectome of Language in Adults: Combined Cortical and Subcortical Single-Subject Analysis Using fMRI and DTI Tractography. Brain Topogr 26, 428–441 (2013). https://doi.org/10.1007/s10548-012-0257-7

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