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The neural architecture of the language comprehension network: converging evidence from lesion and connectivity analyses.

Turken AU, Dronkers NF - Front Syst Neurosci (2011)

Bottom Line: In an earlier voxel-based lesion-symptom mapping analysis of data from aphasic patients (Dronkers et al., 2004), several brain regions in the left hemisphere were found to be critical for language comprehension: the left posterior middle temporal gyrus, the anterior part of Brodmann's area 22 in the superior temporal gyrus (anterior STG/BA22), the posterior superior temporal sulcus (STS) extending into Brodmann's area 39 (STS/BA39), the orbital part of the inferior frontal gyrus (BA47), and the middle frontal gyrus (BA46).The inferior occipito-frontal fasciculus, the arcuate fasciculus, and the middle and inferior longitudinal fasciculi, as well as transcallosal projections via the tapetum were found to be the most prominent white matter pathways bridging the regions important for language comprehension.The left MTG showed a particularly extensive structural and functional connectivity pattern which is consistent with the severity of the impairments associated with MTG lesions and which suggests a central role for this region in language comprehension.

View Article: PubMed Central - PubMed

Affiliation: Department of Veterans Affairs Northern California Health Care System, Center for Aphasia and Related Disorders Martinez, CA, USA.

ABSTRACT
While traditional models of language comprehension have focused on the left posterior temporal cortex as the neurological basis for language comprehension, lesion and functional imaging studies indicate the involvement of an extensive network of cortical regions. However, the full extent of this network and the white matter pathways that contribute to it remain to be characterized. In an earlier voxel-based lesion-symptom mapping analysis of data from aphasic patients (Dronkers et al., 2004), several brain regions in the left hemisphere were found to be critical for language comprehension: the left posterior middle temporal gyrus, the anterior part of Brodmann's area 22 in the superior temporal gyrus (anterior STG/BA22), the posterior superior temporal sulcus (STS) extending into Brodmann's area 39 (STS/BA39), the orbital part of the inferior frontal gyrus (BA47), and the middle frontal gyrus (BA46). Here, we investigated the white matter pathways associated with these regions using diffusion tensor imaging from healthy subjects. We also used resting-state functional magnetic resonance imaging data to assess the functional connectivity profiles of these regions. Fiber tractography and functional connectivity analyses indicated that the left MTG, anterior STG/BA22, STS/BA39, and BA47 are part of a richly interconnected network that extends to additional frontal, parietal, and temporal regions in the two hemispheres. The inferior occipito-frontal fasciculus, the arcuate fasciculus, and the middle and inferior longitudinal fasciculi, as well as transcallosal projections via the tapetum were found to be the most prominent white matter pathways bridging the regions important for language comprehension. The left MTG showed a particularly extensive structural and functional connectivity pattern which is consistent with the severity of the impairments associated with MTG lesions and which suggests a central role for this region in language comprehension.

No MeSH data available.


Related in: MedlinePlus

Functional connectivity profile of the left posterior middle temporal region that was previously found to be critical for the core processes supporting sentence comprehension (Dronkers et al., 2004). The regions that showed highly correlated (p < 0.01, corrected, cluster extent > 100 mm3) spontaneous activity with the left MTG seed are shown on a semi-inflated view of the cortical surface. The left and right hemispheres are shown on the left and right columns, respectively. The upper row shows the lateral surface, and the lower row, the medial surface of the cerebrum. Colors indicate t-values (dark red = lowest, yellow-white = highest, with the voxels within the ROI showing the highest correlation).
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Figure 5: Functional connectivity profile of the left posterior middle temporal region that was previously found to be critical for the core processes supporting sentence comprehension (Dronkers et al., 2004). The regions that showed highly correlated (p < 0.01, corrected, cluster extent > 100 mm3) spontaneous activity with the left MTG seed are shown on a semi-inflated view of the cortical surface. The left and right hemispheres are shown on the left and right columns, respectively. The upper row shows the lateral surface, and the lower row, the medial surface of the cerebrum. Colors indicate t-values (dark red = lowest, yellow-white = highest, with the voxels within the ROI showing the highest correlation).

Mentions: Patients with lesions in MTG and adjacent white matter, including those classified with a severe Wernicke's aphasia, were impaired in all but the simplest sentences, indicating a word-level deficit, which was also confirmed by data from the WAB Auditory Comprehension subtests. Lesions in other areas affected sentence level processing as difficulty level increased (Dronkers et al., 2004, Figure 5), suggesting higher-level contributions to language comprehension. For example, the performance of patients with anterior STG/BA22 lesions declined when the syntactic structure of test items influenced the interpretation of the sentence, suggesting a role for this region in basic morphosyntactic processing. Patients with lesions in frontal regions BA46 and BA47 were impaired only for the most complex sentence structures. The BA47 finding was interpreted as reflecting the impairment of a working memory system for semantic information, whereas the BA46 involvement was attributed to deficits in general cognitive control processes. Finally, posterior STS/BA39 involvement was attributed to auditory short-term memory impairments, as patients with lesions in this region were most impaired on items that relied on auditory rehearsal. Patients whose lesions spared all of these regions showed only minor deficits on the most difficult items. Critically, lesions in the two regions which have traditionally been considered to be at the core of language functioning in the brain, Broca's area (IFG pars opercularis and pars triangularis) and posterior superior temporal gyrus, the cortical zone commonly attributed to Wernicke's area, were not found to be associated with significant language comprehension deficits in this investigation. A small WM region medial to the posterior STS was also identified as being critical for sentence comprehension, suggesting that not only cortical damage but a disconnection produced by a lesion in WM adjacent to posterior STG and MTG might also produce language comprehension deficits.


The neural architecture of the language comprehension network: converging evidence from lesion and connectivity analyses.

Turken AU, Dronkers NF - Front Syst Neurosci (2011)

Functional connectivity profile of the left posterior middle temporal region that was previously found to be critical for the core processes supporting sentence comprehension (Dronkers et al., 2004). The regions that showed highly correlated (p < 0.01, corrected, cluster extent > 100 mm3) spontaneous activity with the left MTG seed are shown on a semi-inflated view of the cortical surface. The left and right hemispheres are shown on the left and right columns, respectively. The upper row shows the lateral surface, and the lower row, the medial surface of the cerebrum. Colors indicate t-values (dark red = lowest, yellow-white = highest, with the voxels within the ROI showing the highest correlation).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3039157&req=5

Figure 5: Functional connectivity profile of the left posterior middle temporal region that was previously found to be critical for the core processes supporting sentence comprehension (Dronkers et al., 2004). The regions that showed highly correlated (p < 0.01, corrected, cluster extent > 100 mm3) spontaneous activity with the left MTG seed are shown on a semi-inflated view of the cortical surface. The left and right hemispheres are shown on the left and right columns, respectively. The upper row shows the lateral surface, and the lower row, the medial surface of the cerebrum. Colors indicate t-values (dark red = lowest, yellow-white = highest, with the voxels within the ROI showing the highest correlation).
Mentions: Patients with lesions in MTG and adjacent white matter, including those classified with a severe Wernicke's aphasia, were impaired in all but the simplest sentences, indicating a word-level deficit, which was also confirmed by data from the WAB Auditory Comprehension subtests. Lesions in other areas affected sentence level processing as difficulty level increased (Dronkers et al., 2004, Figure 5), suggesting higher-level contributions to language comprehension. For example, the performance of patients with anterior STG/BA22 lesions declined when the syntactic structure of test items influenced the interpretation of the sentence, suggesting a role for this region in basic morphosyntactic processing. Patients with lesions in frontal regions BA46 and BA47 were impaired only for the most complex sentence structures. The BA47 finding was interpreted as reflecting the impairment of a working memory system for semantic information, whereas the BA46 involvement was attributed to deficits in general cognitive control processes. Finally, posterior STS/BA39 involvement was attributed to auditory short-term memory impairments, as patients with lesions in this region were most impaired on items that relied on auditory rehearsal. Patients whose lesions spared all of these regions showed only minor deficits on the most difficult items. Critically, lesions in the two regions which have traditionally been considered to be at the core of language functioning in the brain, Broca's area (IFG pars opercularis and pars triangularis) and posterior superior temporal gyrus, the cortical zone commonly attributed to Wernicke's area, were not found to be associated with significant language comprehension deficits in this investigation. A small WM region medial to the posterior STS was also identified as being critical for sentence comprehension, suggesting that not only cortical damage but a disconnection produced by a lesion in WM adjacent to posterior STG and MTG might also produce language comprehension deficits.

Bottom Line: In an earlier voxel-based lesion-symptom mapping analysis of data from aphasic patients (Dronkers et al., 2004), several brain regions in the left hemisphere were found to be critical for language comprehension: the left posterior middle temporal gyrus, the anterior part of Brodmann's area 22 in the superior temporal gyrus (anterior STG/BA22), the posterior superior temporal sulcus (STS) extending into Brodmann's area 39 (STS/BA39), the orbital part of the inferior frontal gyrus (BA47), and the middle frontal gyrus (BA46).The inferior occipito-frontal fasciculus, the arcuate fasciculus, and the middle and inferior longitudinal fasciculi, as well as transcallosal projections via the tapetum were found to be the most prominent white matter pathways bridging the regions important for language comprehension.The left MTG showed a particularly extensive structural and functional connectivity pattern which is consistent with the severity of the impairments associated with MTG lesions and which suggests a central role for this region in language comprehension.

View Article: PubMed Central - PubMed

Affiliation: Department of Veterans Affairs Northern California Health Care System, Center for Aphasia and Related Disorders Martinez, CA, USA.

ABSTRACT
While traditional models of language comprehension have focused on the left posterior temporal cortex as the neurological basis for language comprehension, lesion and functional imaging studies indicate the involvement of an extensive network of cortical regions. However, the full extent of this network and the white matter pathways that contribute to it remain to be characterized. In an earlier voxel-based lesion-symptom mapping analysis of data from aphasic patients (Dronkers et al., 2004), several brain regions in the left hemisphere were found to be critical for language comprehension: the left posterior middle temporal gyrus, the anterior part of Brodmann's area 22 in the superior temporal gyrus (anterior STG/BA22), the posterior superior temporal sulcus (STS) extending into Brodmann's area 39 (STS/BA39), the orbital part of the inferior frontal gyrus (BA47), and the middle frontal gyrus (BA46). Here, we investigated the white matter pathways associated with these regions using diffusion tensor imaging from healthy subjects. We also used resting-state functional magnetic resonance imaging data to assess the functional connectivity profiles of these regions. Fiber tractography and functional connectivity analyses indicated that the left MTG, anterior STG/BA22, STS/BA39, and BA47 are part of a richly interconnected network that extends to additional frontal, parietal, and temporal regions in the two hemispheres. The inferior occipito-frontal fasciculus, the arcuate fasciculus, and the middle and inferior longitudinal fasciculi, as well as transcallosal projections via the tapetum were found to be the most prominent white matter pathways bridging the regions important for language comprehension. The left MTG showed a particularly extensive structural and functional connectivity pattern which is consistent with the severity of the impairments associated with MTG lesions and which suggests a central role for this region in language comprehension.

No MeSH data available.


Related in: MedlinePlus