Aging Affects Neural Synchronization to Speech-Related Acoustic Modulations

Abstract

As people age, speech perception problems become highly prevalent, especially in noisy situations. In addition to peripheral hearing and cognition, temporal processing plays a key role in speech perception. Temporal processing of speech features is mediated by synchronized activity of neural oscillations in the central auditory system. Previous studies indicate that both the degree and hemispheric lateralization of synchronized neural activity relate to speech perception performance. Based on these results, we hypothesize that impaired speech perception in older persons may, in part, originate from deviances in neural synchronization. In this study, auditory steady-state responses that reflect synchronized activity of theta, beta, low and high gamma oscillations (i.e., 4, 20, 40, and 80 Hz ASSR, respectively) were recorded in young, middle-aged, and older persons. As all participants had normal audiometric thresholds and were screened for (mild) cognitive impairment, differences in synchronized neural activity across the three age groups were likely to be attributed to age. Our data yield novel findings regarding theta and high gamma oscillations in the aging auditory system. At an older age, synchronized activity of theta oscillations is increased, whereas high gamma synchronization is decreased. In contrast to young persons who exhibit a right hemispheric dominance for processing of high gamma range modulations, older adults show a symmetrical processing pattern. These age-related changes in neural synchronization may very well underlie the speech perception problems in aging persons.

The effects of aging on neural signatures of temporal regularity processing in sounds

“…ITPC was larger for the regular compared to the random condition for younger (t 29 = 5.666, p < 0.001, r e = 0.725) and older individuals (t 25 = 3.956, p < 0.001, r e = 0.621; Figure 5), but the difference in ITPC between the 'regular' and the 'random' condition was larger in older compared to younger individuals (t 54 = 2.040, p = 0.046, r e = 0.268). This is consistent with previous work showing an enhancement of neural synchronization for amplitude-modulated sounds at low modulation rates for older (>60 years) compared to younger people (<30 years) (Goossens et al, 2016;Presacco et al, 2016a, b). Topographical distributions are consistent with auditory cortex generators (Näätänen and Picton, 1987;Picton et al, 2003).…”

“…How a loss of inhibition and increased responsivity affects the processing of low-frequency temporal regularities such as amplitude modulations in sounds is less well understood. Sensitivity to temporal regularity in sounds can be assessed by the strength of neural synchronization (Purcell et al, 2004;Herrmann et al, 2013a;Goossens et al, 2016;Henry et al, 2017). Neural synchronization reflects the alignment of neural activity with periodicity in sound (Lakatos et al, 2008;Stefanics et al, 2010;Lakatos et al, 2013;Henry and Herrmann, 2014;ten Oever et al, 2017), and is strongest in auditory cortex for low-frequency (<10 Hz) periodicities (Herrmann et al, 2013a;Keitel et al, 2017;Millman et al, 2017).…”

“…Neural synchronization reflects the alignment of neural activity with periodicity in sound (Lakatos et al, 2008;Stefanics et al, 2010;Lakatos et al, 2013;Henry and Herrmann, 2014;ten Oever et al, 2017), and is strongest in auditory cortex for low-frequency (<10 Hz) periodicities (Herrmann et al, 2013a;Keitel et al, 2017;Millman et al, 2017). Some studies report increased synchronization of neural activity with low-frequency amplitude modulations in sounds for older compared to younger humans (Purcell et al, 2004;Goossens et al, 2016;Presacco et al, 2016a) and non-human mammals (Overton and Recanzone, 2016;Herrmann et al, 2017;Lai et al, 2017;Parthasarathy et al, 2019). This enhanced synchronization may reflect a loss of inhibition.…”

“…Age-related changes in neural processing are investigated in three ways: (1) We utilize a stimulus protocol that assesses the temporal dynamics of neural adaptation in auditory cortex, since reduced inhibition in older people may manifest as faster adaptation recovery times in auditory cortex (Herrmann et al, 2016). (2) We assess the tendency for neural activity to synchronize with a sound's amplitude modulation, since reduced inhibition in aging also may also be reflected in enhanced neural synchronization to low-frequency amplitude modulation in sounds (Purcell et al, 2004;Goossens et al, 2016;Presacco et al, 2016a, b;Herrmann et al, 2017). (3) Neural processing that may involve additional higher-level brain regions is assessed using the sustained neural activity in response to the same amplitude-modulated sounds that we utilize to assess sensory gain enhancements.…”

Tonotopic alterations in inhibitory input to the medial nucleus of the trapezoid body in a mouse model of Fragile X syndrome

“…ingly, sound localization deficits have not been rigorously studied in either humans or in a mouse model of FXS. Similar auditory deficits have been seen in other disorders such as central auditory processing disorder (Shamma, 2008) and some forms of age-related hearing loss Goossens, Vercammen, Wouters, & Wieringen, 2016;He, Mills, Ahlstrom, & Dubno, 2008). For these latter conditions, the connection between the symptoms (trouble with sound localization and noisy environment cue disruption) and changes in excitation and inhibition in the sound localization pathway is better understood (Shamma, 2008).…”