Bottom-up and top-down neural signatures of disordered multi-talker speech perception in adults with normal hearing

Abstract

In social settings, speech waveforms from nearby speakers mix together in our ear canals. Normally, the brain unmixes the attended speech stream from the chorus of background speakers using a combination of fast temporal processing and cognitive active listening mechanisms. Of >100,000 patient records,~10% of adults visited our clinic because of reduced hearing, only to learn that their hearing was clinically normal and should not cause communication difficulties. We found that multi-talker speech intelligibility thresholds varied widely in normal hearing adults, but could be predicted from neural phase-locking to frequency modulation (FM) cues measured with ear canal EEG recordings. Combining neural temporal fine structure processing, pupil-indexed listening effort, and behavioral FM thresholds accounted for 78% of the variability in multi-talker speech intelligibility. The disordered bottom-up and top-down markers of poor multi-talker speech perception identified here could inform the design of next-generation clinical tests for hidden hearing disorders.

eLife digest

Our ears were not designed for the society our brains created. The World Health Organization estimates that a billion young adults are at risk for hearing problems due to prolonged exposure to high levels of noise. For many people, the first symptoms of hearing loss consist in an inability to follow a single speaker in crowded places such as restaurants.

However, when Parthasarathy et al. examined over 100,000 records from the Massachusetts Eye and Ear audiology database, they found that around 10% of patients who complained about hearing difficulties were sent home with a clean bill of hearing health. This is because existing tests do not detect common problems related to understanding speech in complex, real-world environments: new tests are needed to spot these hidden hearing disorders. Parthasarathy et al. therefore focused on identifying biological measures that would reflect these issues.

Normally, the brain can ‘unmix’ different speakers and focus on one person, but even in the context of normal hearing, some people are better at this than others. Parthasarathy et al pinpointed several behavioral and biological markers which, when combined, could predict most of this variability. This involved, for example, measuring the diameter of the pupil while people are listening to speech in the presence of several distracting voices (which mirrors how intensively they have to focus on the task) or measuring the participants’ ability to detect subtle changes in frequency (which reflects how fast-changing sound elements are encoded early on in the hearing system). The findings show that an over-reliance on high-level cognitive processes, such as increased listening effort, coupled with problems in the early processing of certain sound traits, was associated with problems in following a speaker in a busy environment.

The biological and behavioral markers highlighted by Parthasarathy et al do not require specialized equipment or marathon sessions to be recorded. In theory, these tests could be implemented into most hospital hearing clinics to give patients and health providers objective data to understand, treat and monitor these hearing difficulties.