Increased listening effort and cochlear neural degeneration underlie behavioral deficits in speech perception in noise in normal hearing middle-aged adults.

Middle-age is a critical period of rapid changes in brain function that presents an opportunity for early diagnostics and intervention for neurodegenerative conditions later in life. Hearing loss is one such early indicator linked to many comorbidities later in life. However, current clinical tests fail to capture hearing difficulties for ~10% of middle-aged adults seeking help at hearing clinics. Cochlear neural degeneration (CND) could play a role in these hearing deficits, but our current understanding is limited by the lack of objective diagnostics and uncertainty regarding its perceptual consequences. Here, using a cross-species approach, we measured envelope following responses (EFRs) - neural ensemble responses to sound originating from the peripheral auditory pathway - in young and middle-aged adults with normal audiometric thresholds, and compared these responses to young and middle-aged Mongolian gerbils, where CND was histologically confirmed. We observed near identical changes in EFRs across species that were associated with CND. Perceptual effects measured as behavioral readouts showed deficits in the most challenging listening conditions and were associated with CND. Additionally, pupil-indexed listening effort increased even at moderate task difficulties where behavioral outcomes were matched. Our results reveal perceptual deficits in middle-aged adults driven by CND and increases in listening effort, which may result in increased listening fatigue and conversational disengagement.

Rapid and objective assessment of auditory temporal processing using dynamic amplitude-modulated stimuli.

Auditory neural coding of speech-relevant temporal cues can be noninvasively probed using envelope following responses (EFRs), neural ensemble responses phase-locked to the stimulus amplitude envelope. EFRs emphasize different neural generators, such as the auditory brainstem or auditory cortex, by altering the temporal modulation rate of the stimulus. EFRs can be an important diagnostic tool to assess auditory neural coding deficits that go beyond traditional audiometric estimations. Existing approaches to measure EFRs use discrete amplitude modulated (AM) tones of varying modulation frequencies, which is time consuming and inefficient, impeding clinical translation. Here we present a faster and more efficient framework to measure EFRs across a range of AM frequencies using stimuli that dynamically vary in modulation rates, combined with spectrally specific analyses that offer optimal spectrotemporal resolution. EFRs obtained from several species (humans, Mongolian gerbils, Fischer-344 rats, and Cba/CaJ mice) showed robust, high-SNR tracking of dynamic AM trajectories (up to 800Hz in humans, and 1.4 kHz in rodents), with a fivefold decrease in recording time and thirtyfold increase in spectrotemporal resolution. EFR amplitudes between dynamic AM stimuli and traditional discrete AM tokens within the same subjects were highly correlated (94% variance explained) across species. Hence, we establish a time-efficient and spectrally specific approach to measure EFRs. These results could yield novel clinical diagnostics for precision audiology approaches by enabling rapid, objective assessment of temporal processing along the entire auditory neuraxis.

Give me a break! Unavoidable fatigue effects in cognitive pupillometry.

Pupillometry has a rich history in the study of perception and cognition. One perennial challenge is that the magnitude of the task-evoked pupil response diminishes over the course of an experiment, a phenomenon we refer to as a fatigue effect. Reducing fatigue effects may improve sensitivity to task effects and reduce the likelihood of confounds due to systematic physiological changes over time. In this paper, we investigated the degree to which fatigue effects could be ameliorated by experimenter intervention. In Experiment 1, we assigned participants to one of three groups-no breaks, kinetic breaks (playing with toys, but no social interaction), or chatting with a research assistant-and compared the pupil response across conditions. In Experiment 2, we additionally tested the effect of researcher observation. Only breaks including social interaction significantly reduced the fatigue of the pupil response across trials. However, in all conditions we found robust evidence for fatigue effects: that is, regardless of protocol, the task-evoked pupil response was substantially diminished (at least 60%) over the duration of the experiment. We account for the variance of fatigue effects in our pupillometry data using multiple common statistical modeling approaches (e.g., linear mixed-effects models of peak, mean, and baseline pupil diameters, as well as growth curve models of time-course data). We conclude that pupil attenuation is a predictable phenomenon that should be accommodated in our experimental designs and statistical models.

Pupillometry reveals cognitive demands of lexical competition during spoken word recognition in young and older adults.

In most contemporary activation-competition frameworks for spoken word recognition, candidate words compete against phonological "neighbors" with similar acoustic properties (e.g., "cap" vs. "cat"). Thus, recognizing words with more competitors should come at a greater cognitive cost relative to recognizing words with fewer competitors, due to increased demands for selecting the correct item and inhibiting incorrect candidates. Importantly, these processes should operate even in the absence of differences in accuracy. In the present study, we tested this proposal by examining differences in processing costs associated with neighborhood density for highly intelligible items presented in quiet. A second goal was to examine whether the cognitive demands associated with increased neighborhood density were greater for older adults compared with young adults. Using pupillometry as an index of cognitive processing load, we compared the cognitive demands associated with spoken word recognition for words with many or fewer neighbors, presented in quiet, for young (n = 67) and older (n = 69) adult listeners. Growth curve analysis of the pupil data indicated that older adults showed a greater evoked pupil response for spoken words than did young adults, consistent with increased cognitive load during spoken word recognition. Words from dense neighborhoods were marginally more demanding to process than words from sparse neighborhoods. There was also an interaction between age and neighborhood density, indicating larger effects of density in young adult listeners. These results highlight the importance of assessing both cognitive demands and accuracy when investigating the mechanisms underlying spoken word recognition.