Dataset Information

Neural organization of speech production: A lesion-based study of error patterns in connected speech.

ABSTRACT: While numerous studies have explored single-word naming, few have evaluated the behavioral and neural correlates of more naturalistic language, like connected speech, which we produce every day. Here, in a retrospective analysis of 120 participants at least six months following left hemisphere stroke, we evaluated the distribution of word errors (paraphasias) and associated brain damage during connected speech (picture description) and object naming. While paraphasias in connected speech and naming shared underlying neural substrates, analysis of the distribution of paraphasias suggested that lexical-semantic load is likely reduced during connected speech. Using voxelwise lesion-symptom mapping (VLSM), we demonstrated that verbal (real word: semantically related and unrelated) and sound (phonemic and neologistic) paraphasias during both connected speech and naming loaded onto the left hemisphere ventral and dorsal streams of language, respectively. Furthermore, for the first time using both connected speech and naming data, we localized semantically related paraphasias to more anterior left hemisphere temporal cortex and unrelated paraphasias to more posterior left temporal and temporoparietal cortex. The connected speech results, in particular, highlight a gradient of specificity as one translates visual recognition from left temporo-occipital cortex to posterior and subsequently anterior temporal cortex. The robustness of VLSM results for sound paraphasias derived during connected speech was notable, in that analyses performed on sound paraphasias from the connected speech task, and not the naming task, demonstrated significant results following removal of lesion volume variance and related apraxia of speech variance. Therefore, connected speech may be a particularly sensitive task on which to evaluate further lexical-phonological processing in the brain. The results presented here demonstrate the related, though different, distribution of paraphasias during connected speech, confirm that paraphasias arising in connected speech and single-word naming likely share neural origins, and endorse the need for continued evaluation of the neural substrates of connected speech processes.

SUBMITTER: Stark BC

PROVIDER: S-EPMC6650360 | biostudies-literature | 2019 Aug

REPOSITORIES: biostudies-literature

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Neural organization of speech production: A lesion-based study of error patterns in connected speech.

Stark Brielle C BC Basilakos Alexandra A Hickok Gregory G Rorden Chris C Bonilha Leonardo L Fridriksson Julius J

Cortex; a journal devoted to the study of the nervous system and behavior 20190307

While numerous studies have explored single-word naming, few have evaluated the behavioral and neural correlates of more naturalistic language, like connected speech, which we produce every day. Here, in a retrospective analysis of 120 participants at least six months following left hemisphere stroke, we evaluated the distribution of word errors (paraphasias) and associated brain damage during connected speech (picture description) and object naming. While paraphasias in connected speech and nam ...[more]

PMID: 31005024

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Project description:Primary progressive aphasia is a clinical syndrome defined by progressive deficits isolated to speech and/or language, and can be classified into non-fluent, semantic and logopenic variants based on motor speech, linguistic and cognitive features. The connected speech of patients with primary progressive aphasia has often been dichotomized simply as 'fluent' or 'non-fluent', however fluency is a multidimensional construct that encompasses features such as speech rate, phrase length, articulatory agility and syntactic structure, which are not always impacted in parallel. In this study, our first objective was to improve the characterization of connected speech production in each variant of primary progressive aphasia, by quantifying speech output along a number of motor speech and linguistic dimensions simultaneously. Secondly, we aimed to determine the neuroanatomical correlates of changes along these different dimensions. We recorded, transcribed and analysed speech samples for 50 patients with primary progressive aphasia, along with neurodegenerative and normal control groups. Patients were scanned with magnetic resonance imaging, and voxel-based morphometry was used to identify regions where atrophy correlated significantly with motor speech and linguistic features. Speech samples in patients with the non-fluent variant were characterized by slow rate, distortions, syntactic errors and reduced complexity. In contrast, patients with the semantic variant exhibited normal rate and very few speech or syntactic errors, but showed increased proportions of closed class words, pronouns and verbs, and higher frequency nouns, reflecting lexical retrieval deficits. In patients with the logopenic variant, speech rate (a common proxy for fluency) was intermediate between the other two variants, but distortions and syntactic errors were less common than in the non-fluent variant, while lexical access was less impaired than in the semantic variant. Reduced speech rate was linked with atrophy to a wide range of both anterior and posterior language regions, but specific deficits had more circumscribed anatomical correlates. Frontal regions were associated with motor speech and syntactic processes, anterior and inferior temporal regions with lexical retrieval, and posterior temporal regions with phonological errors and several other types of disruptions to fluency. These findings demonstrate that a multidimensional quantification of connected speech production is necessary to characterize the differences between the speech patterns of each primary progressive aphasic variant adequately, and to reveal associations between particular aspects of connected speech and specific components of the neural network for speech production.

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

Neural organization of speech production: A lesion-based study of error patterns in connected speech.

Publications

Neural organization of speech production: A lesion-based study of error patterns in connected speech.

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