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Behavioural and neuroanatomical correlates of auditory speech analysis in primary progressive aphasias

BACKGROUND: Non-verbal auditory impairment is increasingly recognised in the primary progressive aphasias (PPAs) but its relationship to speech processing and brain substrates has not been defined. Here we addressed these issues in patients representing the non-fluent variant (nfvPPA) and semantic v...

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Autores principales: Hardy, Chris J. D., Agustus, Jennifer L., Marshall, Charles R., Clark, Camilla N., Russell, Lucy L., Bond, Rebecca L., Brotherhood, Emilie V., Thomas, David L., Crutch, Sebastian J., Rohrer, Jonathan D., Warren, Jason D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5531024/
https://www.ncbi.nlm.nih.gov/pubmed/28750682
http://dx.doi.org/10.1186/s13195-017-0278-2
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author Hardy, Chris J. D.
Agustus, Jennifer L.
Marshall, Charles R.
Clark, Camilla N.
Russell, Lucy L.
Bond, Rebecca L.
Brotherhood, Emilie V.
Thomas, David L.
Crutch, Sebastian J.
Rohrer, Jonathan D.
Warren, Jason D.
author_facet Hardy, Chris J. D.
Agustus, Jennifer L.
Marshall, Charles R.
Clark, Camilla N.
Russell, Lucy L.
Bond, Rebecca L.
Brotherhood, Emilie V.
Thomas, David L.
Crutch, Sebastian J.
Rohrer, Jonathan D.
Warren, Jason D.
author_sort Hardy, Chris J. D.
collection PubMed
description BACKGROUND: Non-verbal auditory impairment is increasingly recognised in the primary progressive aphasias (PPAs) but its relationship to speech processing and brain substrates has not been defined. Here we addressed these issues in patients representing the non-fluent variant (nfvPPA) and semantic variant (svPPA) syndromes of PPA. METHODS: We studied 19 patients with PPA in relation to 19 healthy older individuals. We manipulated three key auditory parameters—temporal regularity, phonemic spectral structure and prosodic predictability (an index of fundamental information content, or entropy)—in sequences of spoken syllables. The ability of participants to process these parameters was assessed using two-alternative, forced-choice tasks and neuroanatomical associations of task performance were assessed using voxel-based morphometry of patients’ brain magnetic resonance images. RESULTS: Relative to healthy controls, both the nfvPPA and svPPA groups had impaired processing of phonemic spectral structure and signal predictability while the nfvPPA group additionally had impaired processing of temporal regularity in speech signals. Task performance correlated with standard disease severity and neurolinguistic measures. Across the patient cohort, performance on the temporal regularity task was associated with grey matter in the left supplementary motor area and right caudate, performance on the phoneme processing task was associated with grey matter in the left supramarginal gyrus, and performance on the prosodic predictability task was associated with grey matter in the right putamen. CONCLUSIONS: Our findings suggest that PPA syndromes may be underpinned by more generic deficits of auditory signal analysis, with a distributed cortico-subcortical neuraoanatomical substrate extending beyond the canonical language network. This has implications for syndrome classification and biomarker development. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13195-017-0278-2) contains supplementary material, which is available to authorized users.
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spelling pubmed-55310242017-08-02 Behavioural and neuroanatomical correlates of auditory speech analysis in primary progressive aphasias Hardy, Chris J. D. Agustus, Jennifer L. Marshall, Charles R. Clark, Camilla N. Russell, Lucy L. Bond, Rebecca L. Brotherhood, Emilie V. Thomas, David L. Crutch, Sebastian J. Rohrer, Jonathan D. Warren, Jason D. Alzheimers Res Ther Research BACKGROUND: Non-verbal auditory impairment is increasingly recognised in the primary progressive aphasias (PPAs) but its relationship to speech processing and brain substrates has not been defined. Here we addressed these issues in patients representing the non-fluent variant (nfvPPA) and semantic variant (svPPA) syndromes of PPA. METHODS: We studied 19 patients with PPA in relation to 19 healthy older individuals. We manipulated three key auditory parameters—temporal regularity, phonemic spectral structure and prosodic predictability (an index of fundamental information content, or entropy)—in sequences of spoken syllables. The ability of participants to process these parameters was assessed using two-alternative, forced-choice tasks and neuroanatomical associations of task performance were assessed using voxel-based morphometry of patients’ brain magnetic resonance images. RESULTS: Relative to healthy controls, both the nfvPPA and svPPA groups had impaired processing of phonemic spectral structure and signal predictability while the nfvPPA group additionally had impaired processing of temporal regularity in speech signals. Task performance correlated with standard disease severity and neurolinguistic measures. Across the patient cohort, performance on the temporal regularity task was associated with grey matter in the left supplementary motor area and right caudate, performance on the phoneme processing task was associated with grey matter in the left supramarginal gyrus, and performance on the prosodic predictability task was associated with grey matter in the right putamen. CONCLUSIONS: Our findings suggest that PPA syndromes may be underpinned by more generic deficits of auditory signal analysis, with a distributed cortico-subcortical neuraoanatomical substrate extending beyond the canonical language network. This has implications for syndrome classification and biomarker development. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13195-017-0278-2) contains supplementary material, which is available to authorized users. BioMed Central 2017-07-27 /pmc/articles/PMC5531024/ /pubmed/28750682 http://dx.doi.org/10.1186/s13195-017-0278-2 Text en © The Author(s). 2017 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Hardy, Chris J. D.
Agustus, Jennifer L.
Marshall, Charles R.
Clark, Camilla N.
Russell, Lucy L.
Bond, Rebecca L.
Brotherhood, Emilie V.
Thomas, David L.
Crutch, Sebastian J.
Rohrer, Jonathan D.
Warren, Jason D.
Behavioural and neuroanatomical correlates of auditory speech analysis in primary progressive aphasias
title Behavioural and neuroanatomical correlates of auditory speech analysis in primary progressive aphasias
title_full Behavioural and neuroanatomical correlates of auditory speech analysis in primary progressive aphasias
title_fullStr Behavioural and neuroanatomical correlates of auditory speech analysis in primary progressive aphasias
title_full_unstemmed Behavioural and neuroanatomical correlates of auditory speech analysis in primary progressive aphasias
title_short Behavioural and neuroanatomical correlates of auditory speech analysis in primary progressive aphasias
title_sort behavioural and neuroanatomical correlates of auditory speech analysis in primary progressive aphasias
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5531024/
https://www.ncbi.nlm.nih.gov/pubmed/28750682
http://dx.doi.org/10.1186/s13195-017-0278-2
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