Age-related deficits in auditory temporal processing: unique contributions of neural dyssynchrony and slowed neuronal processing

Abstract

This study was guided by the hypothesis that the aging central nervous system progressively loses its ability to process rapid acoustic changes that are important for speech recognition. Specifically, we hypothesized that age-related deficits in neural synchrony and neuronal oscillatory activity occur independently in older adults and disrupt auditory temporal processing. Neural synchrony is largely dependent on phase locking within the central auditory pathway, beginning at the auditory nerve. In contrast, the resonance characteristics of oscillatory activity are dependent on the integrity and structure of long range cortical connections. We tested our hypotheses by assessing age-related differences in electrophysiologic correlates of neural synchrony and peak oscillatory frequency in younger and older adults with normal hearing and determining their associations with a behavioral measure of gap detection. Phase-locking values (PLVs) were smaller (poorer neural synchrony) and peak alpha frequency (PAF) was lower for older than younger adults and decreased as gap-detection thresholds increased; variations in PLV and PAF uniquely predicted gap-detection thresholds. These effects were driven, in large part, by associations in older adults. These results reveal dissociable neural mechanisms associated with distinct underlying pathology that may differentially present in older adults and contribute to auditory processing declines.

Consistent pre-stimulus influences on auditory perception across the lifespan

“…Older adults' P1 and N1 component amplitudes were significantly larger compared to younger adults, yet their P2 peaks were reduced. These findings are consistent with previous reports of age-related changes in AEP amplitude (Anderer et al, 1996;Czigler et al, 1992;Harkrider et al, 2005;Henry et al, 2017;Rufener et al, 2014;Tremblay et al, 2003), which may be attributed to age-related changes at the cellular level (Caspary et al, 2008;de Villers-Sidani et al, 2010;Hughes et al, 2010) or neuronal synchrony (Anderson et al, 2012;Harris and Dubno, 2017).…”

“…With advancing age listening becomes more challenging, particularly in "cocktail party" scenarios (de Villers-Sidani et al, 2010;Pichora-Fuller et al, 2017;Rossi-Katz and Arehart, 2009). This difficulty could arise from age-related changes in peripheral and central auditory processes (Anderson et al, 2013;Clinard et al, 2010;Clinard and Cotter, 2015;Harris and Dubno, 2017), such as the poorer encoding in early sensory regions (Grose and Mamo, 2012;He et al, 2007;Mahajan et al, 2017;Paraouty et al, 2016;Wallaert et al, 2016). Changes in higher cognitive processes may also influence older adults' performance via top-down feedback (Henry et al, 2017), through reduced attentional flexibility (Nunez et al, 2015;Zanto and Gazzaley, 2014), or changes in decision criteria when reporting perceptual performance (Dully et al, 2018).…”

Top‐down or bottom up: decreased stimulus salience increases responses to predictable stimuli of auditory thalamic neurons

“…We interpret this as a mechanism for strengthening the internal representations of temporally degraded signals by engaging top-down cognitive resources. Congruent with these interpretations, previous human and animal studies also describe age-related losses in auditory temporal processing and an inability to accurately localize sound in cluttered environments (Pichora-Fuller et al 2007;Dubno et al 2008;Eddins & Hall, 2010;King et al 2014;Harris & Dubno, 2017). Speech in noise conditions degrades speech understanding even in older individuals with healthy hearing (Pichora-Fuller et al 1995).…”

Evidence for independent peripheral and central age‐related hearing impairment

“…The use of the diagnostic term presbycusis ("elderly hearing") to refer to ARHI reflects the common assumption that the speech processing difficulties of older persons should be predictable from their cochlear audiometric configuration (Pacala & Yueh, 2012;Schuknecht & Gacek, 1993). However, clinical interventions aimed at compensating for peripheral hearing loss (e.g., hearing aids) often do not provide adequate benefit for many older patients, suggesting that peripheral and central ARHI are distinct conditions (Gates, 2012;Harris & Dubno, 2017). In humans, however, it is difficult in practice to disentangle the possible interactions between auditory sensory processing and cognitive influences (American Academy Of Audiology, 2010;Humes et al, 2009Humes et al, , 2012Humes et al, , 2013Recanzone, 2018).…”

“…The gap detection threshold (GDT) has been established as the single most common measure of central auditory temporal processing because cognitive influence is minimal, making gap detection potentially ideal for disentangling peripheral and central ARHI (Creelman, 1962;Divenyi & Hirsch, 1974;Preece & Tyler, 1989;Gordon-Salant & Fitzgibbons, 1999;Frisina, 2001;Schoof & Rosen, 2014). Subsequent studies have clearly demonstrated longer GDTs in older populations (Harris & Dubno, 2017;Ozmeral, Eddins, Frisina, & Eddins, 2016;Palmer & Musiek, 2014). However, the question of whether central ARHI could exist independently of peripheral hearing loss remains to be addressed.…”