Electrophysiological and Behavioral Evidence of Reduced Binaural Temporal Processing in the Aging and Hearing Impaired Human Auditory System

Abstract

A person’s ability to process temporal fine structure information is indispensable for speech understanding. As speech understanding typically deteriorates throughout adult life, this study aimed to disentangle age and hearing impairment (HI)-related changes in binaural temporal processing. This was achieved by examining neural and behavioral processing of interaural phase differences (IPDs). Neural IPD processing was studied electrophysiologically through steady-state activity in the electroencephalogram evoked by periodic changes in IPDs over time, embedded in the temporal fine structure of acoustic stimulation. In addition, behavioral IPD discrimination thresholds were determined for the same stimuli. To disentangle potential effects of age from those of HI, both measures were applied to six participant groups: young, middle-aged, and older persons, with either normal hearing or sensorineural HI. All participants passed a cognitive screening, and stimulus audibility was controlled for in participants with HI. The results demonstrated that HI changes neural processing of binaural temporal information for all age-groups included in this study. These outcomes were revealed, superimposed on age-related changes that emerge between young adulthood and middle age. Poorer neural outcomes were also associated with poorer behavioral performance, even though the behavioral IPD discrimination thresholds were affected by age rather than by HI. The neural outcomes of this study are the first to evidence and disentangle the dual load of age and HI on binaural temporal processing. These results could be a valuable first step toward future research on rehabilitation.

Age-Related Deficits in Electrophysiological and Behavioral Measures of Binaural Temporal Processing

“…Similar to findings from studies that used different electrophysiological measurement techniques (Ross et al, 2007a;Ross, 2008;Ozmeral et al, 2016;Papesh et al, 2017;Ungan et al, 2020), Vercammen et al (2018) showed that the neural encoding of IPD cues tends to be stronger in younger participants compared to older participants and, along with several other studies (Haywood et al, 2015;Undurraga et al, 2016;Vercammen et al, 2018;Parthasarathy et al, 2020), showed that IPM-FR responses tend to be weaker when behavioral detection of the IPD cue is poor. While these previous studies have established that the IPM-FR is likely reflective of behavioral IPD sensitivity, the stimuli previously used to assess behavioral IPD discrimination thresholds were dichotic AM stimuli analogous to those used to elicit the IPM-FR (Haywood et al, 2015;Undurraga et al, 2016;Vercammen et al, 2018;Parthasarathy et al, 2020). Assessing relationships between the IPM-FR and other behavioral measures of binaural temporal processing will determine whether associations between the IPM-FR and behavior can generalize to other stimuli and tasks that assess IPD sensitivity.…”

“…This work aimed to (1) confirm previous findings that the IPM-FR, measures of binaural FM detection, and measures of spatial release from masking are sensitive to the effects of age on binaural temporal processing; (2) evaluate associations between the IPM-FR and performance on behavioral measures of IPD sensitivity and speech perception; and (3) explore differences in IPM-FRs elicited using different AM rates. It was predicted that, consistent with previous work (e.g., Grose and Mamo, 2012b;Gallun et al, 2013Gallun et al, , 2014Papesh et al, 2017;Vercammen et al, 2018;Ungan et al, 2020), age would have a significant effect on each neural and behavioral measure of binaural temporal processing, such that older participants would have reduced IPM-FRs, reduced dichotic FM thresholds, and reduced speech understanding abilities compared to younger participants. In addition, it was predicted that older participants would show reduced benefit from the addition of binaural cues in both the FM detection tasks and the spatial release-frommasking tasks compared to younger participants.…”

“…The ability to use these binaural IPD cues is dependent on accurate neural firing to the rapid fluctuations in signal amplitude over time, termed temporal fine structure, and the accurate comparison of these temporal cues between the ears. Recent research has shown that aging can impact the ability to process binaural temporal fine structure information independent of hearing loss, resulting in reduced IPD sensitivity (Ross et al, 2007a;Mamo, 2010, 2012b;Hopkins and Moore, 2011;Gallun et al, 2013Gallun et al, , 2014Papesh et al, 2017;Vercammen et al, 2018) and deficits understanding speech in background noise (Füllgrabe et al, 2015;Papesh et al, 2017). While the exact cause of this age-related decline in temporal processing is unknown, disruptions in neural synchrony, a slowing of neural activity, a loss of cochlear afferent synapses, deficits in the central integration of binaural information, and/or deficits in the central encoding of binaural information have been known to occur with aging (He et al, 2008;Grose and Mamo, 2010;Ruggles et al, 2012;King et al, 2014;Shaheen et al, 2015;Whiteford et al, 2017;Parthasarathy and Kujawa, 2018;Wu et al, 2019).…”

“…Recent reports have focused on the use of non-invasive electrophysiological measures to assess the effects of age on the neural encoding of binaural temporal cues (Ross et al, 2007a;Ross, 2008;Wambacq et al, 2009;Grose and Mamo, 2012a;Ozmeral et al, 2016;Papesh et al, 2017;Eddins and Eddins, 2018;Vercammen et al, 2018;Ungan et al, 2020). For example, Ross et al (2007a) and Papesh et al (2017) recorded transient event-related potentials in response to a 180 • IPD using magnetoencephalography and electroencephalography, respectively.…”

“…The ability to concurrently elicit the ASSR along with the IPM-FR is an additional advantage of this electrophysiological measure, as the ASSR may serve as an estimate of hearing sensitivity (Dimitrijevic et al, 2002;Picton et al, 2003), temporal envelope processing, as well as an index of recording and response quality. Previous studies that have examined the IPM-FR have used stimuli that were amplitude modulated at lower (∼40 Hz; Haywood et al, 2015;Undurraga et al, 2016;Parthasarathy et al, 2020) and higher (∼80 Hz; Vercammen et al, 2018) rates. Although still a source of ongoing investigation (Coffey et al, 2019), it is generally thought that ASSRs elicited using a higher AM rate are primarily generated from more subcortical brainstem structures, including the superior olivary complex and inferior colliculus, while ASSRs elicited using a lower AM rate activate overlapping brainstem structures as well as additional neural generators located in the auditory cortex (Giraud et al, 2000;Herdman et al, 2002;Korczak et al, 2012).…”