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The structural plasticity of white matter networks following anterior temporal lobe resection.

Yogarajah M, Focke NK, Bonelli SB, Thompson P, Vollmar C, McEvoy AW, Alexander DC, Symms MR, Koepp MJ, Duncan JS - Brain (2010)

Bottom Line: These findings were confirmed on analysis of the native clusters and hand drawn regions of interest.The mean pre- and postoperative fractional anisotropy and parallel diffusivity in this cluster were significantly correlated with postoperative verbal fluency and naming test scores.These findings have important implications for our understanding of brain injury and rehabilitation, and may also prove useful in the prediction and minimization of postoperative language deficits.

View Article: PubMed Central - PubMed

Affiliation: Department of Experimental and Clinical Epilepsy, UCL Institute of Neurology, London, WC1N 3BG, UK.

ABSTRACT
Anterior temporal lobe resection is an effective treatment for refractory temporal lobe epilepsy. The structural consequences of such surgery in the white matter, and how these relate to language function after surgery remain unknown. We carried out a longitudinal study with diffusion tensor imaging in 26 left and 20 right temporal lobe epilepsy patients before and a mean of 4.5 months after anterior temporal lobe resection. The whole-brain analysis technique tract-based spatial statistics was used to compare pre- and postoperative data in the left and right temporal lobe epilepsy groups separately. We observed widespread, significant, mean 7%, decreases in fractional anisotropy in white matter networks connected to the area of resection, following both left and right temporal lobe resections. However, we also observed a widespread, mean 8%, increase in fractional anisotropy after left anterior temporal lobe resection in the ipsilateral external capsule and posterior limb of the internal capsule, and corona radiata. These findings were confirmed on analysis of the native clusters and hand drawn regions of interest. Postoperative tractography seeded from this area suggests that this cluster is part of the ventro-medial language network. The mean pre- and postoperative fractional anisotropy and parallel diffusivity in this cluster were significantly correlated with postoperative verbal fluency and naming test scores. In addition, the percentage change in parallel diffusivity in this cluster was correlated with the percentage change in verbal fluency after anterior temporal lobe resection, such that the bigger the increase in parallel diffusivity, the smaller the fall in language proficiency after surgery. We suggest that the findings of increased fractional anisotropy in this ventro-medial language network represent structural reorganization in response to the anterior temporal lobe resection, which may damage the more susceptible dorso-lateral language pathway. These findings have important implications for our understanding of brain injury and rehabilitation, and may also prove useful in the prediction and minimization of postoperative language deficits.

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Group variability map (thresholded at 0.2) of tractography results after seeding from the local maxima of the cluster identified as showing an increase in fractional anisotropy after left anterior temporal lobe resection. Tracts are superimposed upon the MNI152_T1_1mm_brain image supplied with FSL. The group variability map (yellow–red, with yellow representing voxels identified by the tractography in all subjects) visualizes connections from the precentral gyrus via the internal capsule, and connections from the premotor and prefrontal areas, the superior and inferior frontal gyrus (including the deep frontal operculum), which pass via the external capsule to the posterior, superior temporal gyrus and angular gyrus. This network of connections is medial to the traditional dorso-lateral language pathway composed of the arcuate fasciculus and inferior longitudinal fasciculus. The latter pathway is shown for reference in blue and is derived from the JHU white matter tractography atlas supplied with FSL. Also shown is the group variability map for the surgical resection area (dark pink to light pink) created from the postoperative b = 0 images (thresholded at 0.3). It is evident that after an anterior temporal lobe resection the dorso-lateral language connections may be more susceptible to resection and damage than the ventro-medial connections. MNI coordinates are shown on each slice. (DPA = dorsal premotor area; PCG = precentral gyrus; SFG = superior frontal gyrus; EC = external capsule; AG = angular gyrus; FOG = fronto-orbital gyrus; STG = superior temporal gyrus; IFG = inferior frontal gyrus).
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Figure 5: Group variability map (thresholded at 0.2) of tractography results after seeding from the local maxima of the cluster identified as showing an increase in fractional anisotropy after left anterior temporal lobe resection. Tracts are superimposed upon the MNI152_T1_1mm_brain image supplied with FSL. The group variability map (yellow–red, with yellow representing voxels identified by the tractography in all subjects) visualizes connections from the precentral gyrus via the internal capsule, and connections from the premotor and prefrontal areas, the superior and inferior frontal gyrus (including the deep frontal operculum), which pass via the external capsule to the posterior, superior temporal gyrus and angular gyrus. This network of connections is medial to the traditional dorso-lateral language pathway composed of the arcuate fasciculus and inferior longitudinal fasciculus. The latter pathway is shown for reference in blue and is derived from the JHU white matter tractography atlas supplied with FSL. Also shown is the group variability map for the surgical resection area (dark pink to light pink) created from the postoperative b = 0 images (thresholded at 0.3). It is evident that after an anterior temporal lobe resection the dorso-lateral language connections may be more susceptible to resection and damage than the ventro-medial connections. MNI coordinates are shown on each slice. (DPA = dorsal premotor area; PCG = precentral gyrus; SFG = superior frontal gyrus; EC = external capsule; AG = angular gyrus; FOG = fronto-orbital gyrus; STG = superior temporal gyrus; IFG = inferior frontal gyrus).

Mentions: Postoperative tractography from those areas demonstrating an increase in FA after surgery in left anterior temporal lobe resection is shown in Fig. 5. The group variability map of this network of connections consisted of two predominant pathways. Firstly, there was a network of connections running from the precentral gyrus, through the posterior limb of the internal capsule limb to the corticospinal tract and pons. The second pathway consisted of connections from premotor and prefrontal areas, the superior and inferior frontal gyrus (including the deep frontal operculum), and passed via the external capsule to the posterior, superior temporal gyrus and angular gyrus. As this pathway passes through the external capsule, it is ventral and medial to the arcuate fasciculus/superior longitudinal fasciculus whose anatomical location is also shown in Fig. 5 for reference. Part of the distribution of the group variability maps (Fig. 5) approximates to the ventro-medial language network that is distinguishable from the arcuate fasciculus/superior longitudinal fasciculus, which make up the dorso-lateral language network (Saur et al., 2008).Figure 5


The structural plasticity of white matter networks following anterior temporal lobe resection.

Yogarajah M, Focke NK, Bonelli SB, Thompson P, Vollmar C, McEvoy AW, Alexander DC, Symms MR, Koepp MJ, Duncan JS - Brain (2010)

Group variability map (thresholded at 0.2) of tractography results after seeding from the local maxima of the cluster identified as showing an increase in fractional anisotropy after left anterior temporal lobe resection. Tracts are superimposed upon the MNI152_T1_1mm_brain image supplied with FSL. The group variability map (yellow–red, with yellow representing voxels identified by the tractography in all subjects) visualizes connections from the precentral gyrus via the internal capsule, and connections from the premotor and prefrontal areas, the superior and inferior frontal gyrus (including the deep frontal operculum), which pass via the external capsule to the posterior, superior temporal gyrus and angular gyrus. This network of connections is medial to the traditional dorso-lateral language pathway composed of the arcuate fasciculus and inferior longitudinal fasciculus. The latter pathway is shown for reference in blue and is derived from the JHU white matter tractography atlas supplied with FSL. Also shown is the group variability map for the surgical resection area (dark pink to light pink) created from the postoperative b = 0 images (thresholded at 0.3). It is evident that after an anterior temporal lobe resection the dorso-lateral language connections may be more susceptible to resection and damage than the ventro-medial connections. MNI coordinates are shown on each slice. (DPA = dorsal premotor area; PCG = precentral gyrus; SFG = superior frontal gyrus; EC = external capsule; AG = angular gyrus; FOG = fronto-orbital gyrus; STG = superior temporal gyrus; IFG = inferior frontal gyrus).
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Figure 5: Group variability map (thresholded at 0.2) of tractography results after seeding from the local maxima of the cluster identified as showing an increase in fractional anisotropy after left anterior temporal lobe resection. Tracts are superimposed upon the MNI152_T1_1mm_brain image supplied with FSL. The group variability map (yellow–red, with yellow representing voxels identified by the tractography in all subjects) visualizes connections from the precentral gyrus via the internal capsule, and connections from the premotor and prefrontal areas, the superior and inferior frontal gyrus (including the deep frontal operculum), which pass via the external capsule to the posterior, superior temporal gyrus and angular gyrus. This network of connections is medial to the traditional dorso-lateral language pathway composed of the arcuate fasciculus and inferior longitudinal fasciculus. The latter pathway is shown for reference in blue and is derived from the JHU white matter tractography atlas supplied with FSL. Also shown is the group variability map for the surgical resection area (dark pink to light pink) created from the postoperative b = 0 images (thresholded at 0.3). It is evident that after an anterior temporal lobe resection the dorso-lateral language connections may be more susceptible to resection and damage than the ventro-medial connections. MNI coordinates are shown on each slice. (DPA = dorsal premotor area; PCG = precentral gyrus; SFG = superior frontal gyrus; EC = external capsule; AG = angular gyrus; FOG = fronto-orbital gyrus; STG = superior temporal gyrus; IFG = inferior frontal gyrus).
Mentions: Postoperative tractography from those areas demonstrating an increase in FA after surgery in left anterior temporal lobe resection is shown in Fig. 5. The group variability map of this network of connections consisted of two predominant pathways. Firstly, there was a network of connections running from the precentral gyrus, through the posterior limb of the internal capsule limb to the corticospinal tract and pons. The second pathway consisted of connections from premotor and prefrontal areas, the superior and inferior frontal gyrus (including the deep frontal operculum), and passed via the external capsule to the posterior, superior temporal gyrus and angular gyrus. As this pathway passes through the external capsule, it is ventral and medial to the arcuate fasciculus/superior longitudinal fasciculus whose anatomical location is also shown in Fig. 5 for reference. Part of the distribution of the group variability maps (Fig. 5) approximates to the ventro-medial language network that is distinguishable from the arcuate fasciculus/superior longitudinal fasciculus, which make up the dorso-lateral language network (Saur et al., 2008).Figure 5

Bottom Line: These findings were confirmed on analysis of the native clusters and hand drawn regions of interest.The mean pre- and postoperative fractional anisotropy and parallel diffusivity in this cluster were significantly correlated with postoperative verbal fluency and naming test scores.These findings have important implications for our understanding of brain injury and rehabilitation, and may also prove useful in the prediction and minimization of postoperative language deficits.

View Article: PubMed Central - PubMed

Affiliation: Department of Experimental and Clinical Epilepsy, UCL Institute of Neurology, London, WC1N 3BG, UK.

ABSTRACT
Anterior temporal lobe resection is an effective treatment for refractory temporal lobe epilepsy. The structural consequences of such surgery in the white matter, and how these relate to language function after surgery remain unknown. We carried out a longitudinal study with diffusion tensor imaging in 26 left and 20 right temporal lobe epilepsy patients before and a mean of 4.5 months after anterior temporal lobe resection. The whole-brain analysis technique tract-based spatial statistics was used to compare pre- and postoperative data in the left and right temporal lobe epilepsy groups separately. We observed widespread, significant, mean 7%, decreases in fractional anisotropy in white matter networks connected to the area of resection, following both left and right temporal lobe resections. However, we also observed a widespread, mean 8%, increase in fractional anisotropy after left anterior temporal lobe resection in the ipsilateral external capsule and posterior limb of the internal capsule, and corona radiata. These findings were confirmed on analysis of the native clusters and hand drawn regions of interest. Postoperative tractography seeded from this area suggests that this cluster is part of the ventro-medial language network. The mean pre- and postoperative fractional anisotropy and parallel diffusivity in this cluster were significantly correlated with postoperative verbal fluency and naming test scores. In addition, the percentage change in parallel diffusivity in this cluster was correlated with the percentage change in verbal fluency after anterior temporal lobe resection, such that the bigger the increase in parallel diffusivity, the smaller the fall in language proficiency after surgery. We suggest that the findings of increased fractional anisotropy in this ventro-medial language network represent structural reorganization in response to the anterior temporal lobe resection, which may damage the more susceptible dorso-lateral language pathway. These findings have important implications for our understanding of brain injury and rehabilitation, and may also prove useful in the prediction and minimization of postoperative language deficits.

Show MeSH
Related in: MedlinePlus