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

Abstract

BackgroundProcessing 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.MethodsWe 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.ResultsPatients 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.ConclusionsThese 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 materialThe online version of this article (10.1186/s13195-018-0399-2) contains supplementary material, which is available to authorized users.

Impairments of auditory scene analysis in posterior cortical atrophy

“…However, further work is required to characterize the auditory phenotype of PCA more fully, and to evaluate the extent to which ASA impairments constitute a hallmark of Alzheimer's disease pathology; CSF data were only available for 13 patients (62%), meaning that we lacked confirmation of pathophysiology in the remaining eight cases. Emerging evidence suggests that the logopenic variant of primary progressive aphasia, which is typically associated with Alzheimer's disease pathology (Spinelli et al, 2017), may have a specific auditory phenotype (Hardy et al, 2018;Johnson et al, 2020); it remains to be seen whether ASA might also be affected in this patient population. Deficits detected on these psychoacoustic tests across the Alzheimer's disease spectrum should be correlated with structural and functional neuroimaging data to define their neural mechanisms.…”

Anterior temporal lobe is necessary for efficient lateralised processing of spoken word identity

“…For example, SD patients are impaired at distinguishing between real words and non-words in a visual lexical decision task, especially if the non-word in a word/non-word pair (such as FRUIT/FRUTE) follows a more typical orthographic pattern than the word, as measured by bigram and trigram frequencies ( Patterson et al, 2006 ; Rogers, Lambon Ralph, Hodges, & Patterson, 2004 ). Similarly, patients with SD are relatively impaired at identifying acoustically degraded speech in categories for which they have impaired semantic knowledge (place names), compared to those for which their knowledge is intact (number strings) ( Hardy et al, 2018 ), and indeed generally show a striking advantage in verbal working memory for numbers compared to other word-types ( Jefferies, Patterson, Jones, Bateman, & Lambon Ralph, 2004 ).…”

Frontotemporal Dementia: A Clinical Review

“…83,98 To date, the value and feasibility of these strategies remain unproven in FTD. Alongside disease modification, there is a need to develop rational and effective pathophysiologically informed interventions for harnessing residual capacities 99 and controlling symptoms: recent examples include the use of intranasal oxytocin for redressing emotional indifference in FTD syndromes 100 and cognitive rehabilitation and transcranial stimulation techniques in the progressive aphasias. 101,102 Such interventions are likely to become even more relevant as effective diseasemodifying therapies become available.…”