Skip to main content
Top
Published in: Alzheimer's Research & Therapy 1/2018

Open Access 01-12-2018 | Research

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

Authors: Chris J. D. Hardy, Charles R. Marshall, Rebecca L. Bond, Lucy L. Russell, Katrina Dick, Cono Ariti, David L. Thomas, Sonya J. Ross, Jennifer L. Agustus, Sebastian J. Crutch, Jonathan D. Rohrer, Doris-Eva Bamiou, Jason D. Warren

Published in: Alzheimer's Research & Therapy | Issue 1/2018

Login to get access

Abstract

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.
Appendix
Available only for authorised users
Literature
15.
go back to reference Hardy CJD, Hwang YT, Bond RL, Marshall CR, Ridha BH, Crutch SJ, et al. Donepezil enhances understanding of degraded speech in Alzheimer’s disease. Ann Clin Transl Neurol. 2017;4:835–40.CrossRefPubMedPubMedCentral Hardy CJD, Hwang YT, Bond RL, Marshall CR, Ridha BH, Crutch SJ, et al. Donepezil enhances understanding of degraded speech in Alzheimer’s disease. Ann Clin Transl Neurol. 2017;4:835–40.CrossRefPubMedPubMedCentral
36.
37.
go back to reference Davis MH, Johnsrude IS. Hearing speech sounds: top-down influences on the interface between audition and speech perception. Hear Res. 2007;229:132–47.CrossRefPubMed Davis MH, Johnsrude IS. Hearing speech sounds: top-down influences on the interface between audition and speech perception. Hear Res. 2007;229:132–47.CrossRefPubMed
48.
go back to reference Clark CN, Nicholas JM, Agustus JL, Hardy C, Russell L, Brotherhood E, et al. Auditory conflict and congruence in frontotemporal dementia. Neuropsychologia. 2017;104:144–56.CrossRefPubMedPubMedCentral Clark CN, Nicholas JM, Agustus JL, Hardy C, Russell L, Brotherhood E, et al. Auditory conflict and congruence in frontotemporal dementia. Neuropsychologia. 2017;104:144–56.CrossRefPubMedPubMedCentral
52.
go back to reference Goodglass & Weintraub. Kaplan E, Goodglass H, Weintraub S. Boston Naming Test. Philadelphia: Lea & Febiger. 1983. Goodglass & Weintraub. Kaplan E, Goodglass H, Weintraub S. Boston Naming Test. Philadelphia: Lea & Febiger. 1983.
53.
go back to reference Dunn LM & Whetton C. British Picture Vocabulary Scale. Windsor, England: NFER-Nelson. 1997. Dunn LM & Whetton C. British Picture Vocabulary Scale. Windsor, England: NFER-Nelson. 1997.
54.
go back to reference Wechsler D. Wechsler memory scale: Revised. San Antonio, TX: The Psychological Corporation. 1987. Wechsler D. Wechsler memory scale: Revised. San Antonio, TX: The Psychological Corporation. 1987.
55.
go back to reference Jackson M, Warrington EK. Arithmetic skills in patients with unilateral cerebral lesions. Cortex. 1986;22:611–20 Jackson M, Warrington EK. Arithmetic skills in patients with unilateral cerebral lesions. Cortex. 1986;22:611–20
56.
go back to reference Mckenna P, Warrington EK. Testing for nominal dysphasia. J Neurol Neurosurgery, Psychiatry. 1987;43:781–8. Mckenna P, Warrington EK. Testing for nominal dysphasia. J Neurol Neurosurgery, Psychiatry. 1987;43:781–8.
57.
go back to reference Folstein M, Folstein S, McHugh P. “Mini-mental state”: a practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res. 1975;12:189–98. Folstein M, Folstein S, McHugh P. “Mini-mental state”: a practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res. 1975;12:189–98.
58.
go back to reference Kay J, Lesser R, Coltheart M. Psycholinguistic Assessments of Language Processing in Aphasia. Hove, UK: Lawrence Erlbaum Associates; 1996. Kay J, Lesser R, Coltheart M. Psycholinguistic Assessments of Language Processing in Aphasia. Hove, UK: Lawrence Erlbaum Associates; 1996.
59.
go back to reference Warrington EK. Recognition memory test. Windsor: NFER-Nelson; 1984. Warrington EK. Recognition memory test. Windsor: NFER-Nelson; 1984.
60.
go back to reference Warrington E, Mckenna P, Orpwood L. Single Word Comprehension: A Concrete and Abstract Word Synonym Test. Neuropsychol Rehabil. 1998;8:143–54. Warrington E, Mckenna P, Orpwood L. Single Word Comprehension: A Concrete and Abstract Word Synonym Test. Neuropsychol Rehabil. 1998;8:143–54.
61.
go back to reference Tombaugh TN. Trail Making Test A and B: Normative data stratified by age and education. Arch Clin Neuropsychol. 2004;19:203–14. Tombaugh TN. Trail Making Test A and B: Normative data stratified by age and education. Arch Clin Neuropsychol. 2004;19:203–14.
62.
go back to reference Warrington EK, James M. The Visual Object and Space Perception Battery. Bury St Edmunds, UK: Thames Valley Test Company; 1991. Warrington EK, James M. The Visual Object and Space Perception Battery. Bury St Edmunds, UK: Thames Valley Test Company; 1991.
63.
go back to reference Wechsler D. Wechsler Adult Intelligence Scale-Revised. New York: Psychological Corporation; 1981. Wechsler D. Wechsler Adult Intelligence Scale-Revised. New York: Psychological Corporation; 1981.
Metadata
Title
Retained capacity for perceptual learning of degraded speech in primary progressive aphasia and Alzheimer’s disease
Authors
Chris J. D. Hardy
Charles R. Marshall
Rebecca L. Bond
Lucy L. Russell
Katrina Dick
Cono Ariti
David L. Thomas
Sonya J. Ross
Jennifer L. Agustus
Sebastian J. Crutch
Jonathan D. Rohrer
Doris-Eva Bamiou
Jason D. Warren
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Alzheimer's Research & Therapy / Issue 1/2018
Electronic ISSN: 1758-9193
DOI
https://doi.org/10.1186/s13195-018-0399-2

Other articles of this Issue 1/2018

Alzheimer's Research & Therapy 1/2018 Go to the issue