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

Abstract

ABSTRACTSuccessful communication in daily life frequently 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, daily hearing measures (such as degraded speech comprehension) in these diseases remain poorly defined. Here we addressed this issue in a cohort of 19 patients with typical Alzheimer’s disease (AD) and 31 patients representing canonical syndromes of primary progressive aphasia (PPA), in relation to 25 healthy age-matched controls. As a model paradigm for the acoustically degraded speech signals of daily life, we used noise-vocoding: synthetic division of the speech signal into a variable number of 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 MR images) were also assessed. Compared with healthy older controls, all patient groups had a significantly higher mean noise-vocoded speech intelligibility threshold, particularly marked in logopenic variant and nonfluent-agrammatic variant PPA and significantly higher in AD than in semantic variant PPA (all p<0.05). Noise-vocoded intelligibility threshold discriminated dementia syndromes (in particular, Alzheimer’s disease) well from healthy controls. Further, this central hearing measure correlated with overall disease severity but not with measures of peripheral hearing or clear speech perception. Neuroanatomically, after correcting for multiple voxel-wise comparisons in pre-defined regions of interest, impaired noise-vocoded speech comprehension across dementia syndromes was significantly associated (p<0.05) with atrophy of left planum temporale, angular gyrus and anterior cingulate gyrus: a cortical network widely implicated in processing degraded speech signals. Taken together, our findings suggest that the comprehension of acoustically altered speech captures a central process relevant to daily hearing and communication in major dementia syndromes, with novel diagnostic and therapeutic implications.