Aging affects the balance of neural entrainment and top-down neural modulation in the listening brain

Abstract

Healthy aging is accompanied by listening difficulties, including decreased speech comprehension, that stem from an ill-understood combination of sensory and cognitive changes. Here, we use electroencephalography to demonstrate that auditory neural oscillations of older adults entrain less firmly and less flexibly to speech-paced (∼3 Hz) rhythms than younger adults’ during attentive listening. These neural entrainment effects are distinct in magnitude and origin from the neural response to sound per se. Non-entrained parieto-occipital alpha (8–12 Hz) oscillations are enhanced in young adults, but suppressed in older participants, during attentive listening. Entrained neural phase and task-induced alpha amplitude exert opposite, complementary effects on listening performance: higher alpha amplitude is associated with reduced entrainment-driven behavioural performance modulation. Thus, alpha amplitude as a task-driven, neuro-modulatory signal can counteract the behavioural corollaries of neural entrainment. Balancing these two neural strategies may present new paths for intervention in age-related listening difficulties.

“Walking” through the sensory, cognitive, and temporal degradations of healthy aging

“…Hearing impairments due to aging (Table ) lead to various difficulties, such as the loss of the ability to detect, identify, and localize sounds; loss of high‐frequency acuity; slower processing of sounds; difficulty in speech recognition; reduced sensitivity in peripheral hearing; and decreased sensitivity to changes in the temporal envelope and temporal fine structure . Research indicates an approximate mean hearing loss of 50 dB for men and 44 dB for women in the age range of 70–84 years of age, while for individuals over 85 years of age the loss is approximately at 59 and 58 dB, respectively .…”

“…The age‐related decline in auditory processing starts with the loss of hearing sensitivity in higher frequencies that progresses over time to the mid and lower frequencies and has been associated with smaller white matter volume in the areas responsible for auditory and speech processing (e.g., left temporal lobe, right insula, right pre and post gyri) . Additionally, auditory neural oscillations of aging individuals exhibit less flexible entrainment to speech‐paced rhythms (i.e., 3 Hz) as compared to those of young adults . These deficits have been associated with limitations in the activities of daily living, faster cognitive decline, and increased potential for developing depression and dementia …”

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

“…A consequence of peripheral damage is a loss of neural inhibition throughout the auditory system (including cortex) (Caspary et al, 2008;Llano et al, 2012;Takesian et al, 2012;Auerbach et al, 2014). Consistent with a loss of inhibition following peripheral damage, neural responses to sounds are enhanced in the aged and noise-exposed auditory system of animals (Hughes et al, 2010;Chambers et al, 2016;Salvi et al, 2017) and humans (Laffont et al, 1989;Herrmann et al, 2013b;Bidelman et al, 2014;Herrmann et al, 2016;Henry et al, 2017). A loss of inhibition is hypothesized to compensate for reduced inputs from the periphery by up-regulating the responsivity to sound in subcortical and cortical circuits (Caspary et al, 2008;Takesian et al, 2012); this is referred to as central gain enhancement/increase (Auerbach et al, 2014).…”

“…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).…”

Perception of rhythmic speech is modulated by focal bilateral tACS

“…in our sham condition), then this might explain the limited evidence for tACS-induced enhancement of word report in our study. Conversely, impaired neural entrainment has often been reported for hearingimpaired listeners and older individuals (Henry, Herrmann, Kunke, & Obleser, 2017;Petersen, Wöstmann, Obleser, & Lunner, 2017;Presacco, Simon, & Anderson, 2016). It might therefore be that tACS can be used to restore optimal entrainment in impaired listeners who would not achieve optimal entrainment during natural listening.…”