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Surface errors without semantic impairment in acquired dyslexia: a voxel-based lesion-symptom mapping study.

ABSTRACT: Patients with surface dyslexia have disproportionate difficulty pronouncing irregularly spelled words (e.g. pint), suggesting impaired use of lexical-semantic information to mediate phonological retrieval. Patients with this deficit also make characteristic 'regularization' errors, in which an irregularly spelled word is mispronounced by incorrect application of regular spelling-sound correspondences (e.g. reading plaid as 'played'), indicating over-reliance on sublexical grapheme-phoneme correspondences. We examined the neuroanatomical correlates of this specific error type in 45 patients with left hemisphere chronic stroke. Voxel-based lesion-symptom mapping showed a strong positive relationship between the rate of regularization errors and damage to the posterior half of the left middle temporal gyrus. Semantic deficits on tests of single-word comprehension were generally mild, and these deficits were not correlated with the rate of regularization errors. Furthermore, the deep occipital-temporal white matter locus associated with these mild semantic deficits was distinct from the lesion site associated with regularization errors. Thus, in contrast to patients with surface dyslexia and semantic impairment from anterior temporal lobe degeneration, surface errors in our patients were not related to a semantic deficit. We propose that these patients have an inability to link intact semantic representations with phonological representations. The data provide novel evidence for a post-semantic mechanism mediating the production of surface errors, and suggest that the posterior middle temporal gyrus may compute an intermediate representation linking semantics with phonology.

SUBMITTER: Binder JR

PROVIDER: S-EPMC5006249 | biostudies-literature | 2016 May

REPOSITORIES: biostudies-literature

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Surface errors without semantic impairment in acquired dyslexia: a voxel-based lesion-symptom mapping study.

Binder Jeffrey R JR Pillay Sara B SB Humphries Colin J CJ Gross William L WL Graves William W WW Book Diane S DS

Brain : a journal of neurology 20160310 Pt 5

Patients with surface dyslexia have disproportionate difficulty pronouncing irregularly spelled words (e.g. pint), suggesting impaired use of lexical-semantic information to mediate phonological retrieval. Patients with this deficit also make characteristic 'regularization' errors, in which an irregularly spelled word is mispronounced by incorrect application of regular spelling-sound correspondences (e.g. reading plaid as 'played'), indicating over-reliance on sublexical grapheme-phoneme corres ...[more]

PMID: 26966139

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Project description:In the present study, we aimed to test the association between the correct function of the left ventral white matter pathways and semantic processing (dual stream models for language processing, Hickok & Poeppel, 2004), using a new set of language tasks during intraoperative electrical stimulation at white matter level. Additionally, we evaluated brain regions needed for correct performance on the different semantic tasks using lesion-symptom analyses (voxel lesion-symptom mapping and track-wise lesion analysis) in a sample of 62 candidates for the awake brain surgery. We found that electrical stimulation in the vicinity of the inferior longitudinal and inferior fronto-occipital fasciculi disturbed performance on semantic processing tasks. Individuals presented with significantly more semantic paraphasias during brain tumor resection than during the electrical stimulation at the cortex level. Track-wise analyses confirmed the role of these left ventral pathways in semantic processing: a significant relationship was observed between the probability of inferior fronto-occipital fasciculus disconnection/damage and the semantic matching tasks, as well as the number of semantic paraphasias in naming. Importantly, the same analyses for the total score of the Boston Naming Test confirmed significant relationships between this test score and the integrity of the inferior fronto-occipital, inferior longitudinal and uncinate fasciculi. This was further supported by the results of VLSM analyses showing a significant relationship between BNT and the presence of lesion within left middle and inferior temporal gyri. The present findings provide new intraoperative evidence for the role of the white-matter ventral pathways in semantic processing, while at the same time emphasizing the need to include a broader assessment of semantic-conceptual aspects during the awake neurosurgical intervention. This approach will ensure better preservation of functional tissue in the tumoral vicinity and therefore substantially diminish post-surgical language impairments.

Project description:For more than a century, speech repetition has been used as an assay for gauging the integrity of the auditory-motor pathway in aphasia, thought classically to involve a linkage between Wernicke's area and Broca's area via the arcuate fasciculus. During the last decade, evidence primarily from functional imaging in healthy individuals has refined this picture both computationally and anatomically, suggesting the existence of a cortical hub located at the parietal-temporal boundary (area Spt) that functions to integrate auditory and motor speech networks for both repetition and spontaneous speech production. While functional imaging research can pinpoint the regions activated in repetition/auditory-motor integration, lesion-based studies are needed to infer causal involvement. Previous lesion studies of repetition have yielded mixed results with respect to Spt's critical involvement in speech repetition. The present study used voxel-based lesion symptom mapping (VLSM) to investigate the neuroanatomy of repetition of both real words and non-words in a sample of 47 patients with focal left hemisphere brain damage. VLSMs identified a large voxel cluster spanning gray and white matter in the left temporal-parietal junction, including area Spt, where damage was significantly related to poor non-word repetition. Repetition of real words implicated a very similar dorsal network including area Spt. Cortical regions including Spt were implicated in repetition performance even when white matter damage was factored out. In addition, removing variance associated with speech perception abilities did not alter the overall lesion pattern for either task. Together with past functional imaging work, our results suggest that area Spt is integral in both word and non-word repetition, that its contribution is above and beyond that made by white matter pathways, and is not driven by perceptual processes alone. These findings are highly consistent with the claim that Spt is an area of sensory-motor translation in speech processing.

Dataset Information

Surface errors without semantic impairment in acquired dyslexia: a voxel-based lesion-symptom mapping study.

Publications

Surface errors without semantic impairment in acquired dyslexia: a voxel-based lesion-symptom mapping study.

Similar Datasets

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