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Retained capacity for perceptual learning of degraded speech in primary progressive aphasia and Alzheimer’s disease

BACKGROUND: Processing of degraded speech is a promising model for understanding communication under challenging listening conditions, core auditory deficits and residual capacity for perceptual learning and cerebral plasticity in major dementias. METHODS: We compared the processing of sine-wave-deg...

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Autores principales: Hardy, Chris J. D., Marshall, Charles R., Bond, Rebecca L., Russell, Lucy L., Dick, Katrina, Ariti, Cono, Thomas, David L., Ross, Sonya J., Agustus, Jennifer L., Crutch, Sebastian J., Rohrer, Jonathan D., Bamiou, Doris-Eva, Warren, Jason D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6060531/
https://www.ncbi.nlm.nih.gov/pubmed/30045755
http://dx.doi.org/10.1186/s13195-018-0399-2
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author Hardy, Chris J. D.
Marshall, Charles R.
Bond, Rebecca L.
Russell, Lucy L.
Dick, Katrina
Ariti, Cono
Thomas, David L.
Ross, Sonya J.
Agustus, Jennifer L.
Crutch, Sebastian J.
Rohrer, Jonathan D.
Bamiou, Doris-Eva
Warren, Jason D.
author_facet Hardy, Chris J. D.
Marshall, Charles R.
Bond, Rebecca L.
Russell, Lucy L.
Dick, Katrina
Ariti, Cono
Thomas, David L.
Ross, Sonya J.
Agustus, Jennifer L.
Crutch, Sebastian J.
Rohrer, Jonathan D.
Bamiou, Doris-Eva
Warren, Jason D.
author_sort Hardy, Chris J. D.
collection PubMed
description BACKGROUND: Processing of degraded speech is a promising model for understanding communication under challenging listening conditions, core auditory deficits and residual capacity for perceptual learning and cerebral plasticity in major dementias. METHODS: We compared the processing of sine-wave-degraded speech in 26 patients with primary progressive aphasia (non-fluent, semantic, and logopenic variants), 10 patients with typical Alzheimer’s disease and 17 healthy control subjects. Participants were required to identify sine-wave words that were more predictable (three-digit numbers) or less predictable (place names). The change in identification performance within each session indexed perceptual learning. Neuroanatomical associations of degraded speech processing were assessed using voxel-based morphometry. RESULTS: Patients with non-fluent and logopenic progressive aphasia and typical Alzheimer’s disease showed impaired identification of sine-wave numbers, whereas all syndromic groups showed impaired identification of sine-wave place names. A significant overall identification advantage for numbers over place names was shown by patients with typical Alzheimer’s disease, patients with semantic progressive aphasia and healthy control participants. All syndromic groups showed spontaneous perceptual learning effects for sine-wave numbers. For the combined patient cohort, grey matter correlates were identified across a distributed left hemisphere network extending beyond classical speech-processing cortices. CONCLUSIONS: These findings demonstrate resilience of auditory perceptual learning capacity across dementia syndromes, despite variably impaired perceptual decoding of degraded speech and reduced predictive integration of semantic knowledge. This work has implications for the neurobiology of dynamic sensory processing and plasticity in neurodegenerative diseases and for development of novel biomarkers and therapeutic interventions. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13195-018-0399-2) contains supplementary material, which is available to authorized users.
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spelling pubmed-60605312018-07-31 Retained capacity for perceptual learning of degraded speech in primary progressive aphasia and Alzheimer’s disease Hardy, Chris J. D. Marshall, Charles R. Bond, Rebecca L. Russell, Lucy L. Dick, Katrina Ariti, Cono Thomas, David L. Ross, Sonya J. Agustus, Jennifer L. Crutch, Sebastian J. Rohrer, Jonathan D. Bamiou, Doris-Eva Warren, Jason D. Alzheimers Res Ther Research BACKGROUND: Processing of degraded speech is a promising model for understanding communication under challenging listening conditions, core auditory deficits and residual capacity for perceptual learning and cerebral plasticity in major dementias. METHODS: We compared the processing of sine-wave-degraded speech in 26 patients with primary progressive aphasia (non-fluent, semantic, and logopenic variants), 10 patients with typical Alzheimer’s disease and 17 healthy control subjects. Participants were required to identify sine-wave words that were more predictable (three-digit numbers) or less predictable (place names). The change in identification performance within each session indexed perceptual learning. Neuroanatomical associations of degraded speech processing were assessed using voxel-based morphometry. RESULTS: Patients with non-fluent and logopenic progressive aphasia and typical Alzheimer’s disease showed impaired identification of sine-wave numbers, whereas all syndromic groups showed impaired identification of sine-wave place names. A significant overall identification advantage for numbers over place names was shown by patients with typical Alzheimer’s disease, patients with semantic progressive aphasia and healthy control participants. All syndromic groups showed spontaneous perceptual learning effects for sine-wave numbers. For the combined patient cohort, grey matter correlates were identified across a distributed left hemisphere network extending beyond classical speech-processing cortices. CONCLUSIONS: These findings demonstrate resilience of auditory perceptual learning capacity across dementia syndromes, despite variably impaired perceptual decoding of degraded speech and reduced predictive integration of semantic knowledge. This work has implications for the neurobiology of dynamic sensory processing and plasticity in neurodegenerative diseases and for development of novel biomarkers and therapeutic interventions. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13195-018-0399-2) contains supplementary material, which is available to authorized users. BioMed Central 2018-07-25 /pmc/articles/PMC6060531/ /pubmed/30045755 http://dx.doi.org/10.1186/s13195-018-0399-2 Text en © The Author(s). 2018 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.
Marshall, Charles R.
Bond, Rebecca L.
Russell, Lucy L.
Dick, Katrina
Ariti, Cono
Thomas, David L.
Ross, Sonya J.
Agustus, Jennifer L.
Crutch, Sebastian J.
Rohrer, Jonathan D.
Bamiou, Doris-Eva
Warren, Jason D.
Retained capacity for perceptual learning of degraded speech in primary progressive aphasia and Alzheimer’s disease
title Retained capacity for perceptual learning of degraded speech in primary progressive aphasia and Alzheimer’s disease
title_full Retained capacity for perceptual learning of degraded speech in primary progressive aphasia and Alzheimer’s disease
title_fullStr Retained capacity for perceptual learning of degraded speech in primary progressive aphasia and Alzheimer’s disease
title_full_unstemmed Retained capacity for perceptual learning of degraded speech in primary progressive aphasia and Alzheimer’s disease
title_short Retained capacity for perceptual learning of degraded speech in primary progressive aphasia and Alzheimer’s disease
title_sort retained capacity for perceptual learning of degraded speech in primary progressive aphasia and alzheimer’s disease
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6060531/
https://www.ncbi.nlm.nih.gov/pubmed/30045755
http://dx.doi.org/10.1186/s13195-018-0399-2
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