Age-related hearing loss increases full-brain connectivity while reversing directed signaling within the dorsal–ventral pathway for speech

Abstract

Speech comprehension difficulties are ubiquitous to aging and hearing loss, particularly in noisy environments. Older adults' poorer speech-in-noise (SIN) comprehension has been related to abnormal neural representations within various nodes (regions) of the speech network, but how senescent changes in hearing alter the transmission of brain signals remains unspecified. We measured electroencephalograms in older adults with and without mild hearing loss during a SIN identification task. Using functional connectivity and graph-theoretic analyses, we show that hearing-impaired (HI) listeners have more extended (less integrated) communication pathways and less efficient information exchange among widespread brain regions (larger network eccentricity) than their normal-hearing (NH) peers. Parameter optimized support vector machine classifiers applied to EEG connectivity data showed hearing status could be decoded (> 85% accuracy) solely using network-level descriptions of brain activity, but classification was particularly robust using left hemisphere connections. Notably, we found a reversal in directed neural signaling in left hemisphere dependent on hearing status among specific connections within the dorsalventral speech pathways. NH listeners showed an overall net "bottom-up" signaling directed from auditory cortex (A1) to inferior frontal gyrus (IFG; Broca's area), whereas the HI group showed the reverse signal (i.e., "top-down" Broca's → A1). A similar flow reversal was noted between

Decoding Hearing-Related Changes in Older Adults’ Spatiotemporal Neural Processing of Speech Using Machine Learning

“…Analyses of the ERPs and behavioral data associated with this dataset are reported elsewhere ( Bidelman et al, 2019a , b ). In this study, we present a new machine learning analysis to identify the most discriminating spatiotemporal features of full-brain neuroelectric activity that best segregates NH and mild hearing loss listeners in terms of their SIN processing.…”

“…The task lasted ∼20 min. Analysis of the behavioral data associated with this task are reported elsewhere (Bidelman et al, 2019a).…”

“…Although we adopt widely used clinic criteria, there is typically large individual differences in older adults speech perception even with a similar (or even normal) audiogram (Konkle et al, 1977;van Rooij and Plomp, 1992;Gordon-Salant and Fitzgibbons, 1993;Cruickshanks et al, 1998;Strouse et al, 1998;Schneider et al, 2002;Hutka et al, 2013). However, behaviorally, our older HI listeners showed little decrement in speech detection accuracy relative to their NH peers, although they were more variable on standardize measures of SIN perception (i.e., QuickSIN test) (Bidelman et al, 2019a). Still, future studies are needed to determine (i) if our brain decoding results generalize to more severe (or even undiagnosed) hearing losses, (ii) scale with individual differences in perceptual skills, and (iii) might change with cognitive decline that is common in older adults (e.g., .…”

“…In noisy environments, left inferior frontal gyrus and left inferior parietal lobe are recruited for speech perception (Dimitrijevic et al, 2019). In our earlier EEG studies (Bidelman et al, 2019a;Price et al, 2019), we used functional connectivity analysis to demonstrate that older listeners with mild hearing loss had more extended (less integrated) communication pathways and less efficient information exchange across the brain than their NH peers; directed connectivity analysis further showed that age-related HI reverses the direction of neural signaling within important hubs of the auditory-linguistic-motor loop of the dorsal-ventral pathways (e.g., primary auditory cortexinferior frontal gyrus -primary motor cortex), implying a rerouting of information within the same speech circuitry (Bidelman et al, 2019a).…”

“…In older adults, HI has been associated with poor cognitive health, social isolation, and loneliness ( Lin et al, 2013 ; Diaz et al, 2018 ). Speech processing in the elderly relies on a complex network of interacting brain regions ( Hickok and Poeppel, 2004 , 2007 ; Rauschecker and Scott, 2009 ; Bidelman et al, 2019a ). Age-related HI is thought to occur due to a myriad of changes in both the central auditory pathways ( Bidelman et al, 2014 , 2019b ) and widespread areas of both cerebral hemispheres ( Gates and Mills, 2005 ).…”