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Neural organization of spoken language revealed by lesion-symptom mapping.

Mirman D, Chen Q, Zhang Y, Wang Z, Faseyitan OK, Coslett HB, Schwartz MF - Nat Commun (2015)

Bottom Line: In this study, we combine high-quality structural neuroimaging analysis techniques and extensive behavioural assessment of patients with persistent acquired language deficits to study the neural basis of language.Phonological form deficits are associated with lesions in peri-Sylvian regions, whereas semantic production and recognition deficits are associated with damage to the left anterior temporal lobe and white matter connectivity with frontal cortex, respectively.These findings provide a novel synthesis of traditional and contemporary views of the cognitive and neural architecture of language processing, emphasizing dual routes for speech processing and convergence of white matter tracts for semantic control and/or integration.

View Article: PubMed Central - PubMed

Affiliation: 1] Moss Rehabilitation Research Institute, 50 Township Line Road, Elkins Park, Pennsylvania 19027, USA [2] Department of Psychology, Drexel University, 3141 Chestnut Street, Philadelphia, Pennsylvania 19104, USA.

ABSTRACT
Studies of patients with acquired cognitive deficits following brain damage and studies using contemporary neuroimaging techniques form two distinct streams of research on the neural basis of cognition. In this study, we combine high-quality structural neuroimaging analysis techniques and extensive behavioural assessment of patients with persistent acquired language deficits to study the neural basis of language. Our results reveal two major divisions within the language system-meaning versus form and recognition versus production-and their instantiation in the brain. Phonological form deficits are associated with lesions in peri-Sylvian regions, whereas semantic production and recognition deficits are associated with damage to the left anterior temporal lobe and white matter connectivity with frontal cortex, respectively. These findings provide a novel synthesis of traditional and contemporary views of the cognitive and neural architecture of language processing, emphasizing dual routes for speech processing and convergence of white matter tracts for semantic control and/or integration.

No MeSH data available.


Related in: MedlinePlus

VLSM of Semantic RecognitionVLSM of Semantic Recognition factor scores with direct total lesion volume control. Voxels exceeding FDR threshold q = 0.1 are shown in red superimposed on outlines of key white matter tracts: uncinate fasciculus (light blue), inferior fronto-occipital fasciculus (green), and anterior thalamic radiations (blue). Far right panel shows a tractography reconstruction of these tracts and the supra-threshold voxels using the same color scheme. See Methods for details of white matter rendering.
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Figure 3: VLSM of Semantic RecognitionVLSM of Semantic Recognition factor scores with direct total lesion volume control. Voxels exceeding FDR threshold q = 0.1 are shown in red superimposed on outlines of key white matter tracts: uncinate fasciculus (light blue), inferior fronto-occipital fasciculus (green), and anterior thalamic radiations (blue). Far right panel shows a tractography reconstruction of these tracts and the supra-threshold voxels using the same color scheme. See Methods for details of white matter rendering.

Mentions: VLSM of the Semantic Recognition factor identified no voxels in the ATL, even at a relaxed q = 0.1 FDR threshold (Fig. 3). Nor were there voxels in any other cortical region typically associated with semantic processing, such as middle temporal gyrus or angular gyrus9,24. Instead, the identified voxels were primarily in the white matter medial to the insula and lateral to the basal ganglia. Several white matter tracts converge in this region, including the inferior fronto-occipital fasciculus (IFOF), the uncinate fasciculus (UNC), and the anterior thalamic radiations (ATR). The region did not include the superior longitudinal fasciculus (SLF III, which on some accounts corresponds to the fronto-parietal portion of the arcuate fasciculus25): the SLF/AF passes dorsally to this region26 or, on some accounts27, terminates posterior to it. The convergence of major white matter tracts in the identified area creates a “bottleneck” where a small amount of damage can cause a large degree of dysfunction in connections between frontal cortices and the rest of the brain. The association with the semantic recognition factor likely owes to the fact that semantic cognition requires integration across multiple regions of a distributed cortical network9,21. Our proposal is that damage to the bottleneck region disrupts connectivity between the frontal lobe and other brain regions involved in semantic processing, consistent with other recent findings28–30.


Neural organization of spoken language revealed by lesion-symptom mapping.

Mirman D, Chen Q, Zhang Y, Wang Z, Faseyitan OK, Coslett HB, Schwartz MF - Nat Commun (2015)

VLSM of Semantic RecognitionVLSM of Semantic Recognition factor scores with direct total lesion volume control. Voxels exceeding FDR threshold q = 0.1 are shown in red superimposed on outlines of key white matter tracts: uncinate fasciculus (light blue), inferior fronto-occipital fasciculus (green), and anterior thalamic radiations (blue). Far right panel shows a tractography reconstruction of these tracts and the supra-threshold voxels using the same color scheme. See Methods for details of white matter rendering.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4400840&req=5

Figure 3: VLSM of Semantic RecognitionVLSM of Semantic Recognition factor scores with direct total lesion volume control. Voxels exceeding FDR threshold q = 0.1 are shown in red superimposed on outlines of key white matter tracts: uncinate fasciculus (light blue), inferior fronto-occipital fasciculus (green), and anterior thalamic radiations (blue). Far right panel shows a tractography reconstruction of these tracts and the supra-threshold voxels using the same color scheme. See Methods for details of white matter rendering.
Mentions: VLSM of the Semantic Recognition factor identified no voxels in the ATL, even at a relaxed q = 0.1 FDR threshold (Fig. 3). Nor were there voxels in any other cortical region typically associated with semantic processing, such as middle temporal gyrus or angular gyrus9,24. Instead, the identified voxels were primarily in the white matter medial to the insula and lateral to the basal ganglia. Several white matter tracts converge in this region, including the inferior fronto-occipital fasciculus (IFOF), the uncinate fasciculus (UNC), and the anterior thalamic radiations (ATR). The region did not include the superior longitudinal fasciculus (SLF III, which on some accounts corresponds to the fronto-parietal portion of the arcuate fasciculus25): the SLF/AF passes dorsally to this region26 or, on some accounts27, terminates posterior to it. The convergence of major white matter tracts in the identified area creates a “bottleneck” where a small amount of damage can cause a large degree of dysfunction in connections between frontal cortices and the rest of the brain. The association with the semantic recognition factor likely owes to the fact that semantic cognition requires integration across multiple regions of a distributed cortical network9,21. Our proposal is that damage to the bottleneck region disrupts connectivity between the frontal lobe and other brain regions involved in semantic processing, consistent with other recent findings28–30.

Bottom Line: In this study, we combine high-quality structural neuroimaging analysis techniques and extensive behavioural assessment of patients with persistent acquired language deficits to study the neural basis of language.Phonological form deficits are associated with lesions in peri-Sylvian regions, whereas semantic production and recognition deficits are associated with damage to the left anterior temporal lobe and white matter connectivity with frontal cortex, respectively.These findings provide a novel synthesis of traditional and contemporary views of the cognitive and neural architecture of language processing, emphasizing dual routes for speech processing and convergence of white matter tracts for semantic control and/or integration.

View Article: PubMed Central - PubMed

Affiliation: 1] Moss Rehabilitation Research Institute, 50 Township Line Road, Elkins Park, Pennsylvania 19027, USA [2] Department of Psychology, Drexel University, 3141 Chestnut Street, Philadelphia, Pennsylvania 19104, USA.

ABSTRACT
Studies of patients with acquired cognitive deficits following brain damage and studies using contemporary neuroimaging techniques form two distinct streams of research on the neural basis of cognition. In this study, we combine high-quality structural neuroimaging analysis techniques and extensive behavioural assessment of patients with persistent acquired language deficits to study the neural basis of language. Our results reveal two major divisions within the language system-meaning versus form and recognition versus production-and their instantiation in the brain. Phonological form deficits are associated with lesions in peri-Sylvian regions, whereas semantic production and recognition deficits are associated with damage to the left anterior temporal lobe and white matter connectivity with frontal cortex, respectively. These findings provide a novel synthesis of traditional and contemporary views of the cognitive and neural architecture of language processing, emphasizing dual routes for speech processing and convergence of white matter tracts for semantic control and/or integration.

No MeSH data available.


Related in: MedlinePlus