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

Abstract 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 se...

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Main Authors: Chris J. D. Hardy, Jennifer L. Agustus, Charles R. Marshall, Camilla N. Clark, Lucy L. Russell, Rebecca L. Bond, Emilie V. Brotherhood, David L. Thomas, Sebastian J. Crutch, Jonathan D. Rohrer, Jason D. Warren
Format: Article
Language:English
Published: BMC 2017-07-01
Series:Alzheimer’s Research & Therapy
Subjects:
Online Access:http://link.springer.com/article/10.1186/s13195-017-0278-2
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spelling doaj-330088e3d5074a669c1e7fb5c727e7ce2020-11-25T02:16:44ZengBMCAlzheimer’s Research & Therapy1758-91932017-07-019111010.1186/s13195-017-0278-2Behavioural and neuroanatomical correlates of auditory speech analysis in primary progressive aphasiasChris J. D. Hardy0Jennifer L. Agustus1Charles R. Marshall2Camilla N. Clark3Lucy L. Russell4Rebecca L. Bond5Emilie V. Brotherhood6David L. Thomas7Sebastian J. Crutch8Jonathan D. Rohrer9Jason D. Warren10Dementia Research Centre, Department of Neurodegenerative Disease, UCL Institute of Neurology, University College LondonDementia Research Centre, Department of Neurodegenerative Disease, UCL Institute of Neurology, University College LondonDementia Research Centre, Department of Neurodegenerative Disease, UCL Institute of Neurology, University College LondonDementia Research Centre, Department of Neurodegenerative Disease, UCL Institute of Neurology, University College LondonDementia Research Centre, Department of Neurodegenerative Disease, UCL Institute of Neurology, University College LondonDementia Research Centre, Department of Neurodegenerative Disease, UCL Institute of Neurology, University College LondonDementia Research Centre, Department of Neurodegenerative Disease, UCL Institute of Neurology, University College LondonDementia Research Centre, Department of Neurodegenerative Disease, UCL Institute of Neurology, University College LondonDementia Research Centre, Department of Neurodegenerative Disease, UCL Institute of Neurology, University College LondonDementia Research Centre, Department of Neurodegenerative Disease, UCL Institute of Neurology, University College LondonDementia Research Centre, Department of Neurodegenerative Disease, UCL Institute of Neurology, University College LondonAbstract 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.http://link.springer.com/article/10.1186/s13195-017-0278-2SpeechAuditoryVoxel-based morphometryPrimary progressive aphasiaSemantic dementiaProgressive non-fluent aphasia
collection DOAJ
language English
format Article
sources DOAJ
author Chris J. D. Hardy
Jennifer L. Agustus
Charles R. Marshall
Camilla N. Clark
Lucy L. Russell
Rebecca L. Bond
Emilie V. Brotherhood
David L. Thomas
Sebastian J. Crutch
Jonathan D. Rohrer
Jason D. Warren
spellingShingle Chris J. D. Hardy
Jennifer L. Agustus
Charles R. Marshall
Camilla N. Clark
Lucy L. Russell
Rebecca L. Bond
Emilie V. Brotherhood
David L. Thomas
Sebastian J. Crutch
Jonathan D. Rohrer
Jason D. Warren
Behavioural and neuroanatomical correlates of auditory speech analysis in primary progressive aphasias
Alzheimer’s Research & Therapy
Speech
Auditory
Voxel-based morphometry
Primary progressive aphasia
Semantic dementia
Progressive non-fluent aphasia
author_facet Chris J. D. Hardy
Jennifer L. Agustus
Charles R. Marshall
Camilla N. Clark
Lucy L. Russell
Rebecca L. Bond
Emilie V. Brotherhood
David L. Thomas
Sebastian J. Crutch
Jonathan D. Rohrer
Jason D. Warren
author_sort Chris J. D. Hardy
title 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_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_sort behavioural and neuroanatomical correlates of auditory speech analysis in primary progressive aphasias
publisher BMC
series Alzheimer’s Research & Therapy
issn 1758-9193
publishDate 2017-07-01
description Abstract 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.
topic Speech
Auditory
Voxel-based morphometry
Primary progressive aphasia
Semantic dementia
Progressive non-fluent aphasia
url http://link.springer.com/article/10.1186/s13195-017-0278-2
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