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Combined DTI Tractography and Functional MRI Study of the Language Connectome in Healthy Volunteers: Extensive Mapping of White Matter Fascicles and Cortical Activations.

Vassal F, Schneider F, Boutet C, Jean B, Sontheimer A, Lemaire JJ - PLoS ONE (2016)

Bottom Line: Eight putative WM fascicles for language were probed using a deterministic DTI-FT technique: the arcuate fascicle (AF), superior longitudinal fascicle (SLF), uncinate fascicle (UF), temporo-occipital fascicle, inferior fronto-occipital fascicle (IFOF), middle longitudinal fascicle (MdLF), frontal aslant fascicle and operculopremotor fascicle.WM fascicle terminations were also observed beyond fMRI-confirmed language areas and reached numerous cortical areas involved in different functional brain networks.These findings suggest that the reported WM fascicles are not exclusively involved in language and might be related to other cognitive functions such as visual recognition, spatial attention, executive functions, memory, and processing of emotional and behavioral aspects.

View Article: PubMed Central - PubMed

Affiliation: IGCNC (Image-Guided Clinical Neuroscience and Connectomics), EA 7282, Unité de Formation et de Recherche Médecine, Université d'Auvergne, Clermont-Ferrand, France.

ABSTRACT
Despite a better understanding of brain language organization into large-scale cortical networks, the underlying white matter (WM) connectivity is still not mastered. Here we combined diffusion tensor imaging (DTI) fiber tracking (FT) and language functional magnetic resonance imaging (fMRI) in twenty healthy subjects to gain new insights into the macroscopic structural connectivity of language. Eight putative WM fascicles for language were probed using a deterministic DTI-FT technique: the arcuate fascicle (AF), superior longitudinal fascicle (SLF), uncinate fascicle (UF), temporo-occipital fascicle, inferior fronto-occipital fascicle (IFOF), middle longitudinal fascicle (MdLF), frontal aslant fascicle and operculopremotor fascicle. Specific measurements (i.e. volume, length, fractional anisotropy) and precise cortical terminations were derived for each WM fascicle within both hemispheres. Connections between these WM fascicles and fMRI activations were studied to determine which WM fascicles are related to language. WM fascicle volumes showed asymmetries: leftward for the AF, temporoparietal segment of SLF and UF, and rightward for the frontoparietal segment of the SLF. The lateralization of the AF, IFOF and MdLF extended to differences in patterns of anatomical connections, which may relate to specific hemispheric abilities. The leftward asymmetry of the AF was correlated to the leftward asymmetry of fMRI activations, suggesting that the lateralization of the AF is a structural substrate of hemispheric language dominance. We found consistent connections between fMRI activations and terminations of the eight WM fascicles, providing a detailed description of the language connectome. WM fascicle terminations were also observed beyond fMRI-confirmed language areas and reached numerous cortical areas involved in different functional brain networks. These findings suggest that the reported WM fascicles are not exclusively involved in language and might be related to other cognitive functions such as visual recognition, spatial attention, executive functions, memory, and processing of emotional and behavioral aspects.

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Labeling of cortical terminations according to anatomical landmarks.Cortical terminations of white matter fascicles (e.g. left arcuate fascicle; green) were labeled according to gyri and sulci provided by 3D surface renderings (A) generated from high-resolution T1-weighted magnetic resonance images (B; sagittal section running through the left frontal operculum). a = horizontal ramus of the Sylvian fissure; b = ascending ramus of the Sylvian fissure; c = precentral sulcus; d = central sulcus; e = superior temporal sulcus; 1 = pars orbitalis of the inferior frontal gyrus (Brodmann area [BA] 47); 2 = pars triangularis (BA 45); 3 = pars opercularis (BA 44); 4 = ventral premotor cortex (BA 6); 5 = precentral gyrus (BA 4/6); 6 = superior temporal gyrus (BA 22); 7 = middle temporal gyrus (BA 21).
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pone.0152614.g002: Labeling of cortical terminations according to anatomical landmarks.Cortical terminations of white matter fascicles (e.g. left arcuate fascicle; green) were labeled according to gyri and sulci provided by 3D surface renderings (A) generated from high-resolution T1-weighted magnetic resonance images (B; sagittal section running through the left frontal operculum). a = horizontal ramus of the Sylvian fissure; b = ascending ramus of the Sylvian fissure; c = precentral sulcus; d = central sulcus; e = superior temporal sulcus; 1 = pars orbitalis of the inferior frontal gyrus (Brodmann area [BA] 47); 2 = pars triangularis (BA 45); 3 = pars opercularis (BA 44); 4 = ventral premotor cortex (BA 6); 5 = precentral gyrus (BA 4/6); 6 = superior temporal gyrus (BA 22); 7 = middle temporal gyrus (BA 21).

Mentions: Image datasets were co-registered (mutual information algorithm) using iPlan Stereotaxy 3.0 software. The FA, color-coded direction, and BOLD-cluster maps were co-registered with T1-weighted MR images (anatomical reference). Accuracy of registration was carefully reviewed (visual analysis of merged images and test-retests) using the following landmarks: putamen, pallidum, corpus callosum (whole body and major and minor forceps), anterior and posterior limbs of the internal capsule, cerebellar contour, tentorium of the posterior fossa, sylvian region, upper brainstem contour, ventricular system (frontal horns and trigone), interhemispheric fissure and main cerebral gyrations. For each individual, we generated 3D surface renderings of the brain from T1-weighted MR images used to determine the cortical terminations of WM fascicles within the frontal, parietal, temporal and occipital lobes of the right and left hemispheres. Cortical territories were labeled according to classical anatomical terminology, as follows (Fig 2): frontal pole (FP, BA 10); lateral (lOrbF, BA 11) and medial (mOrbF, BA 12) orbitofrontal cortex; subgenual cortex (SubG, BA 25); SMA (dorsal part of BA 6); MFG (BA 9/46); Broca’s area, located in the pars opercularis, triangularis and orbitalis of the IFG (BA 44/45/47); vPMC (ventral part of BA 6); superior parietal lobule (SPL, BA 7); precuneus (PCN, BA 7); Geschwind’s area, located in the IPL including the AG (BA 39) and SMG (BA 40) gyrus; TP (BA 38); parahippocampal gyrus (PHG, BA 28); uncus (UNC, BA 34); Wernicke’s area, located in the pMTG/pSTG (BA 21/22); inferior temporal gyrus (ITG, BA 20); temporo-occipital cortex including the fusiform gyrus (T-O, BA 37); and occipital lobe (OL) including cuneus (CN), lingual gyrus and lateral occipital gyri (BA 18/19).


Combined DTI Tractography and Functional MRI Study of the Language Connectome in Healthy Volunteers: Extensive Mapping of White Matter Fascicles and Cortical Activations.

Vassal F, Schneider F, Boutet C, Jean B, Sontheimer A, Lemaire JJ - PLoS ONE (2016)

Labeling of cortical terminations according to anatomical landmarks.Cortical terminations of white matter fascicles (e.g. left arcuate fascicle; green) were labeled according to gyri and sulci provided by 3D surface renderings (A) generated from high-resolution T1-weighted magnetic resonance images (B; sagittal section running through the left frontal operculum). a = horizontal ramus of the Sylvian fissure; b = ascending ramus of the Sylvian fissure; c = precentral sulcus; d = central sulcus; e = superior temporal sulcus; 1 = pars orbitalis of the inferior frontal gyrus (Brodmann area [BA] 47); 2 = pars triangularis (BA 45); 3 = pars opercularis (BA 44); 4 = ventral premotor cortex (BA 6); 5 = precentral gyrus (BA 4/6); 6 = superior temporal gyrus (BA 22); 7 = middle temporal gyrus (BA 21).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4814138&req=5

pone.0152614.g002: Labeling of cortical terminations according to anatomical landmarks.Cortical terminations of white matter fascicles (e.g. left arcuate fascicle; green) were labeled according to gyri and sulci provided by 3D surface renderings (A) generated from high-resolution T1-weighted magnetic resonance images (B; sagittal section running through the left frontal operculum). a = horizontal ramus of the Sylvian fissure; b = ascending ramus of the Sylvian fissure; c = precentral sulcus; d = central sulcus; e = superior temporal sulcus; 1 = pars orbitalis of the inferior frontal gyrus (Brodmann area [BA] 47); 2 = pars triangularis (BA 45); 3 = pars opercularis (BA 44); 4 = ventral premotor cortex (BA 6); 5 = precentral gyrus (BA 4/6); 6 = superior temporal gyrus (BA 22); 7 = middle temporal gyrus (BA 21).
Mentions: Image datasets were co-registered (mutual information algorithm) using iPlan Stereotaxy 3.0 software. The FA, color-coded direction, and BOLD-cluster maps were co-registered with T1-weighted MR images (anatomical reference). Accuracy of registration was carefully reviewed (visual analysis of merged images and test-retests) using the following landmarks: putamen, pallidum, corpus callosum (whole body and major and minor forceps), anterior and posterior limbs of the internal capsule, cerebellar contour, tentorium of the posterior fossa, sylvian region, upper brainstem contour, ventricular system (frontal horns and trigone), interhemispheric fissure and main cerebral gyrations. For each individual, we generated 3D surface renderings of the brain from T1-weighted MR images used to determine the cortical terminations of WM fascicles within the frontal, parietal, temporal and occipital lobes of the right and left hemispheres. Cortical territories were labeled according to classical anatomical terminology, as follows (Fig 2): frontal pole (FP, BA 10); lateral (lOrbF, BA 11) and medial (mOrbF, BA 12) orbitofrontal cortex; subgenual cortex (SubG, BA 25); SMA (dorsal part of BA 6); MFG (BA 9/46); Broca’s area, located in the pars opercularis, triangularis and orbitalis of the IFG (BA 44/45/47); vPMC (ventral part of BA 6); superior parietal lobule (SPL, BA 7); precuneus (PCN, BA 7); Geschwind’s area, located in the IPL including the AG (BA 39) and SMG (BA 40) gyrus; TP (BA 38); parahippocampal gyrus (PHG, BA 28); uncus (UNC, BA 34); Wernicke’s area, located in the pMTG/pSTG (BA 21/22); inferior temporal gyrus (ITG, BA 20); temporo-occipital cortex including the fusiform gyrus (T-O, BA 37); and occipital lobe (OL) including cuneus (CN), lingual gyrus and lateral occipital gyri (BA 18/19).

Bottom Line: Eight putative WM fascicles for language were probed using a deterministic DTI-FT technique: the arcuate fascicle (AF), superior longitudinal fascicle (SLF), uncinate fascicle (UF), temporo-occipital fascicle, inferior fronto-occipital fascicle (IFOF), middle longitudinal fascicle (MdLF), frontal aslant fascicle and operculopremotor fascicle.WM fascicle terminations were also observed beyond fMRI-confirmed language areas and reached numerous cortical areas involved in different functional brain networks.These findings suggest that the reported WM fascicles are not exclusively involved in language and might be related to other cognitive functions such as visual recognition, spatial attention, executive functions, memory, and processing of emotional and behavioral aspects.

View Article: PubMed Central - PubMed

Affiliation: IGCNC (Image-Guided Clinical Neuroscience and Connectomics), EA 7282, Unité de Formation et de Recherche Médecine, Université d'Auvergne, Clermont-Ferrand, France.

ABSTRACT
Despite a better understanding of brain language organization into large-scale cortical networks, the underlying white matter (WM) connectivity is still not mastered. Here we combined diffusion tensor imaging (DTI) fiber tracking (FT) and language functional magnetic resonance imaging (fMRI) in twenty healthy subjects to gain new insights into the macroscopic structural connectivity of language. Eight putative WM fascicles for language were probed using a deterministic DTI-FT technique: the arcuate fascicle (AF), superior longitudinal fascicle (SLF), uncinate fascicle (UF), temporo-occipital fascicle, inferior fronto-occipital fascicle (IFOF), middle longitudinal fascicle (MdLF), frontal aslant fascicle and operculopremotor fascicle. Specific measurements (i.e. volume, length, fractional anisotropy) and precise cortical terminations were derived for each WM fascicle within both hemispheres. Connections between these WM fascicles and fMRI activations were studied to determine which WM fascicles are related to language. WM fascicle volumes showed asymmetries: leftward for the AF, temporoparietal segment of SLF and UF, and rightward for the frontoparietal segment of the SLF. The lateralization of the AF, IFOF and MdLF extended to differences in patterns of anatomical connections, which may relate to specific hemispheric abilities. The leftward asymmetry of the AF was correlated to the leftward asymmetry of fMRI activations, suggesting that the lateralization of the AF is a structural substrate of hemispheric language dominance. We found consistent connections between fMRI activations and terminations of the eight WM fascicles, providing a detailed description of the language connectome. WM fascicle terminations were also observed beyond fMRI-confirmed language areas and reached numerous cortical areas involved in different functional brain networks. These findings suggest that the reported WM fascicles are not exclusively involved in language and might be related to other cognitive functions such as visual recognition, spatial attention, executive functions, memory, and processing of emotional and behavioral aspects.

Show MeSH
Related in: MedlinePlus