Cited by 28Dementia and Cognitive Impairment ResearchHearing Loss and RehabilitationNeurobiology of Language and Bilingualism

Comprehension of acoustically degraded speech in Alzheimer’s disease and primary progressive aphasia

Open access
Jiang, Jessica, Johnson, Jeremy C S, Requena-Komuro, Maï-Carmen, Benhamou, Elia, Sivasathiaseelan, Harri, Chokesuwattanaskul, Anthipa, Nelson, Annabel, Nortley, Ross +6 more·2023·Brain

Published version of a preprint

Abstract

Successful communication in daily life depends on accurate decoding of speech signals that are acoustically degraded by challenging listening conditions. This process presents the brain with a demanding computational task that is vulnerable to neurodegenerative pathologies. However, despite recent intense interest in the link between hearing impairment and dementia, comprehension of acoustically degraded speech in these diseases has been little studied. Here we addressed this issue in a cohort of 19 patients with typical Alzheimer's disease and 30 patients representing the three canonical syndromes of primary progressive aphasia (non-fluent/agrammatic variant primary progressive aphasia; semantic variant primary progressive aphasia; logopenic variant primary progressive aphasia), compared to 25 healthy age-matched controls. As a paradigm for the acoustically degraded speech signals of daily life, we used noise-vocoding: synthetic division of the speech signal into frequency channels constituted from amplitude-modulated white noise, such that fewer channels convey less spectrotemporal detail thereby reducing intelligibility. We investigated the impact of noise-vocoding on recognition of spoken three-digit numbers and used psychometric modelling to ascertain the threshold number of noise-vocoding channels required for 50% intelligibility by each participant. Associations of noise-vocoded speech intelligibility threshold with general demographic, clinical and neuropsychological characteristics and regional grey matter volume (defined by voxel-based morphometry of patients' brain images) were also assessed. Mean noise-vocoded speech intelligibility threshold was significantly higher in all patient groups than healthy controls, and significantly higher in Alzheimer's disease and logopenic variant primary progressive aphasia than semantic variant primary progressive aphasia (all P < 0.05). In a receiver operating characteristic analysis, vocoded intelligibility threshold discriminated Alzheimer's disease, non-fluent variant and logopenic variant primary progressive aphasia patients very well from healthy controls. Further, this central hearing measure correlated with overall disease severity but not with peripheral hearing or clear speech perception. Neuroanatomically, after correcting for multiple voxel-wise comparisons in predefined regions of interest, impaired noise-vocoded speech comprehension across syndromes was significantly associated (P < 0.05) with atrophy of left planum temporale, angular gyrus and anterior cingulate gyrus: a cortical network that has previously been widely implicated in processing degraded speech signals. Our findings suggest that the comprehension of acoustically altered speech captures an auditory brain process relevant to daily hearing and communication in major dementia syndromes, with novel diagnostic and therapeutic implications.

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  • Novel speech perception paradigms capture syndrome-differential deficits by manipulating temporal and spectral properties of recorded speech.

    “Promising avenues for cross-linguistic research also come from novel speech perception paradigms, which capture syndrome-differential deficits by manipu lating temporal and spectral properties of recorded speech. 126-128”

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  1. [34]Gates GA, Mills JH. Presbycusis. Lancet. 2005; 366: 1111– 1120. 16182900
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  3. [91]Johnson JCS. Hearing impairment in dementia: Defining deficits and assessing impact. PhD thesis. University College London; 2021.

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Authors
Jiang, J., Johnson, J. C. S., Requena-Komuro, M.-C., Benhamou, E., Sivasathiaseelan, H., Chokesuwattanaskul, A., Nelson, A., Nortley, R., Weil, R. S., Volkmer, A., Marshall, C. R., Bamiou, D.-E., Warren, J. D., & Hardy, C. J. D.
Affiliations
  • UCL Queen Square Institute of Neurology (GB)
  • Dementia Research Centre, Department of Neurodegenerative Disease, UCL Queen Square Institute of Neurology, University College London , London WC1N 3AR , UK
  • Thai Red Cross Society (TH)
  • Wexham Park Hospital (GB)
  • University College London (GB)
  • Queen Mary University of London (GB)
  • UCL Biomedical Research Centre (GB)
Corresponding author
Hardy, Chris J D
Venue
Brain
Published
2023-05-15
Volume
146
Issue
10
Pages
4065-4076
ISSN
  • 0006-8950 (ISSN-L)
  • 1460-2156
OpenAlex
W4376618147
Cited by
28
References
92
Citations by year
2026: 8 · 2025: 13 · 2024: 5 · 2023: 2
FWCI
5.68
Type
journal article
Language
en
Open access
Locations
  • Brain (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Queen Mary Research Online (Queen Mary University of London) (submittedVersion, cc-by)
Funders
  • The Dementia Research Centre
  • Alzheimer’s Research UK
  • Brain Research Trust
  • The Wolfson Foundation
  • Alzheimer’s Society (AS-PG-16-007)
  • the Royal National Institute for Deaf People, Alzheimer’s Research UK
  • National Institute for Health Research University College London Hospitals Biomedical Research Centre
  • the Wellcome Trust (102129/B/13/Z)
  • UK Research and Innovation
  • Creative Commons Attribution
  • Frontotemporal Dementia Research Studentship in Memory of David Blechner
  • The National Brain Appeal
  • Association of British Neurologists Clinical Research Training Fellowship
  • Wellcome Trust PhD studentship (102129/B/13/Z)
  • Brain Research UK PhD Studentship
  • Clinical Research Fellowship
  • Leonard Wolfson Experimental Neurology Centre
  • NIHR Advanced Fellowship (NIHR302240)
  • Bart’s Charity and the National Institute for Health Research (NIHR204280)
  • Wellcome Clinical Research Career Development Fellowship (205167/Z/16/Z)
  • Royal National Institute for Deaf People
  • RNID-Dunhill Medical Trust Pauline Ashley Fellowship (PA23_Hardy)
  • Wellcome Institutional Strategic Support Fund Award (204841/Z/16/Z)
  • National Institute for Health Research (NIHR204280)
  • NIHR [Invention for Innovation (NIHR204280)
  • NIHR
  • Department of Health and Social Care
Topics
  • Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Hearing Loss and Rehabilitation
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neurobiology of Language and Bilingualism
Keywords
speech understanding, Alzheimer's disease, primary progressive aphasia, noise-vocoded speech, dementia, logopenic variant primary progressive aphasia, semantic dementia, planum temporale, angular gyrus, anterior cingulate cortex, gray matter atrophy, auditory cortex, hearing loss
MeSH terms
Alzheimer Disease, Aphasia, Brain, Humans, Neuropsychological Tests, Speech, Aphasia, Primary Progressive, Comprehension

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