The Effect of Aging, Parkinson’s Disease, and Exogenous Dopamine on the Neural Response Associated with Auditory Regularity Processing

Abstract

Processing regular patterns in auditory scenes is important for navigating complex environments. Electroencephalography (EEG) studies find enhancement of sustained brain activity, correlating with the emergence of a regular pattern in sounds. How aging, aging-related diseases such as Parkinson's disease (PD), and treatment of PD affect this fundamental function remain unknown. We addressed this knowledge gap. Healthy younger and older adults, and PD patients listened to sounds that contained or were devoid of regular patterns. Healthy older adults and PD patients were tested twice-on and off dopaminergic medication in counterbalanced order.Regularity-evoked, sustained EEG activity was reduced in older, compared to younger adults. PD patients and older controls had comparable attenuation of the sustained response. Dopaminergic therapy further weakened the sustained response in both groups. These findings suggest that fundamental regularity processing is impacted by aging-related neural changes but not those underlying PD. The finding that dopaminergic therapy attenuates rather than improves the sustained response coheres with the dopamine overdose response and implicates brain regions receiving dopamine from the ventral tegmental area in regularity processing.

A Neural Signature of Regularity in Sound is Reduced in Older Adults

“…Hence, although neural responses to the onset of sound was enhanced in older adults, neural sensitivity to a pattern in sounds was reduced. Diminished sustained activity for older compared to younger adults is consistent with previous indications of an age-related reduction in sustained activity for short (<1 s) pure tones (Pfefferbaum et al, 1979), amplitude modulations (Herrmann et al, 2019), and repeated patterns in tone sequences (Al Jaja et al, 2020). However, low statistical reliability and differences in stimulus parameters between age groups did not allow drawing firm conclusions from the latter two studies.…”

“…More recent work indicates that younger individuals exhibit pattern-related sustained activity in response to amplitude-modulated sounds, whereas older adults do not appear to, although the difference between these groups was not significant (Herrmann et al, 2019). Another study yielded data suggestive of reduced sustained activity in older compared to younger people in response to repeated tone sequences (Al Jaja et al, 2020), but stimulus parameters differed between age groups in this paper. A controlled experiment with sufficient power is thus required to elucidate whether sustained neural activity to regular sound patterns differs between younger and older people.…”

“…Previous work investigating sustained neural activity in older adults has utilized low-density electroencephalography (EEG; fewer than 20 electrodes; Pfefferbaum et al, 1979; Herrmann et al, 2019; Al Jaja et al, 2020). This type of EEG is not very well suited for the localization of neural sources generating scalp-recorded signals.…”

Sustained responses and neural synchronization to amplitude and frequency modulation in sound change with age

“…The original degrees of freedom, epsilon coefficient, and corrected p-value are reported. All participants were included in the analysis of the sustained response, since the more intense stimuli presented to older people would lead to larger responses, if anything, and we hypothesized that sustained activity would be reduced in older compared to younger adults (Pfefferbaum et al, 1979; Al Jaja et al, 2020; Herrmann et al, 2022).…”

“…For example, short pure tones elicited a smaller sustained response in older compared to younger adults (Pfefferbaum et al, 1979). The sustained neural response elicited by repeated sets of tones in longer tone sequences has also been shown to be reduced for older relative to younger adults (Al Jaja et al, 2020; Herrmann et al, 2022). A similar age-related reduction in the sustained response has been reported in an EEG study for low-frequency amplitude modulations (Herrmann et al, 2019), although the effect of age group (younger vs older) was only marginally significant in this study.…”