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

Abstract

Sensitivity to repetitions in sound amplitude and frequency is crucial for sound perception. As with other aspects of sound processing, sensitivity to such patterns may change with age, and may help explain some age-related changes in hearing such as segregating speech from background sound. We recorded magnetoencephalography to characterize differences in the processing of sound patterns between younger and older adults. We presented tone sequences that either contained a pattern (made of a repeated set of tones) or did not contain a pattern. We show that auditory cortex in older, compared to younger, adults is hyperresponsive to sound onsets, but that sustained neural activity in auditory cortex, indexing the processing of a sound pattern, is reduced. Hence, the sensitivity of neural populations in auditory cortex fundamentally differs between younger and older individuals, overresponding to sound onsets, while underresponding to patterns in sounds. This may help to explain some age-related changes in hearing such as increased sensitivity to distracting sounds and difficulties tracking speech in the presence of other sound.

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

“…In order to obtain a reference threshold in MATLAB software for sound presentation during the main experimental procedures, we also estimated the sensation level for a narrow-band noise that was generated similarly to the sounds used in the current study (see below), using a method-of-limits procedure (Herrmann et al, 2022). Participants listened to a 15-s narrow-band noise (~0.84–2.6 kHz) that changed continuously in intensity at a rate of 4 dB/s (either decreased [i.e., starting at suprathreshold levels] or increased [i.e., starting at subthreshold levels]).…”

“…To approximately match audibility across age groups, all sound stimuli presented during the main experiment (described below) were presented at 55 dB above each individual’s sensation level (Herrmann et al, 2022). Since sensation levels and audiometric thresholds were on average larger for older compared to younger adults, sounds presented during the main experiment were on average more intense in sound-pressure level in older compared to younger adults.…”

“…The study was conducted in accordance with the Declaration of Helsinki and the Canadian Tri-Council Policy Statement on Ethical Conduct for Research Involving Humans, and was approved by the Nonmedical Research Ethics Board of the University of Western Ontario. Additional data (~12 min) for a different project (Herrmann et al, 2022) were recorded during each of the two each sessions. Apart from audiometric hearing thresholds, none of the data reported here have been published previously.…”

“…The sustained response is an ultralow-frequency response (i.e., a constant or slowly drifting offset) elicited by the occurrence of a temporally regular pattern in a sound. A sustained response has been demonstrated in response to repeated sets of pure tones in longer sequences of tones (Barascud et al, 2016; Southwell et al, 2017; Herrmann and Johnsrude, 2018; Southwell and Chait, 2018; Herrmann et al, 2022), coherent frequency changes in multi-tone chords (Teki et al, 2016; Dheerendra et al, 2021), and complex sounds made of isochronous tone sequences (Sohoglu and Chait, 2016). A sustained response has also been observed for amplitude (Ross et al, 2002; Herrmann et al, 2019) and frequency modulations in sounds (Herrmann and Johnsrude, 2018), and for isochronously presented clicks or vowels compared to irregular presentations (Gutschalk et al, 2002; Gutschalk and Uppenkamp, 2011).…”

“…The consequence of reduced inhibition and increased excitation is hyperactivity and hyperresponsivity to suprathreshold sounds, particularly at the level of auditory cortex (Auerbach et al, 2014; Salvi et al, 2017; Herrmann and Butler, 2021a). In EEG/MEG recordings, hyperresponsivity is prominently represented as larger auditory cortex responses to sound onset for older compared to younger adults or for adults with hearing loss compared to adults without (Ross and Tremblay, 2009; Sörös et al, 2009; Lister et al, 2011; Alain et al, 2014; Bidelman et al, 2014; Parry et al, 2019; Irsik et al, 2021; Herrmann et al, 2022).…”