Available online 17 May 2024, 109034

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Aging results in reduced midbrain phase locking but increased cortical amplitudes.

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Reduced afferent input contributes to overcompensation in auditory cortex.

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Midbrain and cortical temporal processing contribute to the ability to identify single words that differ in transition durations.

ABSTRACT

Older listeners have particular difficulty processing temporal cues that are important for word discrimination, and deficient processing may limit their ability to benefit from these cues. Here, we investigated aging effects on perception and neural representation of the consonant transition and the factors that contribute to successful perception. To further understand the neural mechanisms underlying the changes in processing from brainstem to cortex, we also examined the factors that contribute to exaggerated amplitudes in cortex. We enrolled 30 younger normal-hearing and 30 older normal-hearing participants who met the criteria of clinically normal hearing. Perceptual identification functions were obtained for the words BEAT and WHEAT on a 7-step continuum of consonant-transition duration. Auditory brainstem responses (ABRs) were recorded to click stimuli and frequency-following responses (FFRs) and cortical auditory-evoked potentials were recorded to the endpoints of the BEAT-WHEAT continuum. Perceptual performance for identification of BEAT vs. WHEAT did not differ between younger and older listeners. However, both subcortical and cortical measures of neural representation showed age group differences, such that FFR phase locking was lower but cortical amplitudes (P1 and N1) were higher in older compared to younger listeners. ABR Wave I amplitude and FFR phase locking, but not audiometric thresholds, predicted early cortical amplitudes. Phase locking to the transition region and early cortical peak amplitudes (P1) predicted performance on the perceptual identification function. Overall results suggest that the neural representation of transition durations and cortical overcompensation may contribute to the ability to perceive transition duration contrasts. Cortical overcompensation appears to be a maladaptive response to decreased neural firing/synchrony.

Section snippetsINTRODUCTION

Older adults often report having difficulty understanding speech in challenging listening situations. They state that they can hear their conversation partners speaking but that their partners’ words lack clarity. These difficulties may arise in part from temporal processing deficits that reduce access to the fast temporal cues that are characteristic of speech signals (reviewed in Anderson and Karawani, 2020). Sensitivity to temporal cues can be assessed by measuring the listener's perception

MATERIALS AND METHODS

Participants: Participants comprised older (55-76 years of age, mean = 63, S.D. = 4.6, n = 30, M = 8) and younger (18-24 years of age, mean = 21, S.D. = 2.1, n = 30, M = 5) listeners with clinically normal audiometric thresholds (Figure 1). This sample size was based on an effect size of 0.45 calculated from (Roque et al., 2019b). A mixed-effect regression analysis with six factors, an alpha level of 0.05 and a power level of 0.80 specified 52 participants, and we recruited 60 participants to

Audiometric test results

Figure 1 displays mean thresholds and standard deviations of audiometric thresholds from 1.25 to 14 kHz. The mean pure-tone average (PTA, average threshold from 2 to 8 kHz) in the YNH group was 3.43 dB (± 4.5 S.D.) and was significantly different from that of the ONH group 12.87 dB (± 4.6 S.D.) (t = 8.05, p < 0.001). The mean high-frequency pure-tone average (HFPTA, average threshold from 8 to 12.5 kHz) in the YNH group was -0.93 dB (± 5.3 S.D.) and was also significantly different from that of

Cortical

Linear mixed-effects models were performed with CAEP amplitude and latency as predicted variables and the following fixed factors: Age group, Word, Peak (P1, N1, and P2), and their interactions. The amplitude and latency values were calculated from the DSS analysis.

Amplitude: Figure 6 displays grand average waveforms generated from the DSS analysis and from the Cz electrode. Table 5 shows the results of the final best-fitting model for cortical amplitude. There was a main effect of Age group (t

Summary

The results supported some, but not all our initial hypotheses. Aging effects were seen for subcortical and cortical neural encoding (Figure 3, Figure 4, Figure 5, Figure 6), but not for perception of transition duration contrasts (Fig. 2). Phase locking to the transition region was a significant factor in perceptual performance. Wave I amplitude and PLF, but not hearing thresholds, contributed significantly to cortical P1 amplitude, supporting the idea that reduced afferent input activates

Cortical

Similar to the ABR findings, there were no age effects on cortical latencies, but there were significant age effects on cortical amplitudes that varied by peak. The early peaks represent pre-perceptual signal detection (P1; Ceponiene et al., 2005; Sharma et al., 2002) and triggering of neural attention (N1; Ceponiene et al., 2002; Näätänen, 1990), and P2 amplitude is associated with auditory object identification (Näätänen and Winkler, 1999; Ross et al., 2013). Amplitudes of P1 and N1 were

Perceptual-Neural relationships

Peripheral (Wave I) and central factors (PLF and P1 amplitude) were included in a model to predict the ability to detect changes in transition duration. There was an overall effect of phase locking on performance, such that higher PLF values were associated with higher numbers of BEAT responses at shorter transition durations and lower numbers of BEAT responses at longer durations. P1 amplitude also modified responses at shorter transition durations, such that lower amplitudes were associated

Conclusion

These results have ramifications for clinical management of individuals who report hearing difficulties, with or without audiometrically measured hearing loss. A decrease in neural synchrony at auditory nerve and midbrain levels leads to cortical compensation, especially in older adults. This compensation seems to be a homeostatic shift in the balance of inhibitory and excitatory neurotransmission in response to decreased or degraded afferent input. Inhibition is necessary for the brain's

Funding Information

This study was supported by the National Institute on Deafness and Other Communication Disorders of the National Institutes of Health (NIH) under award number

R21DC015843 (Anderson). The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

Compliance with ethical standards

The authors declare that they have no conflicts of interests.

Author statement

Abigail Poe: Formal analysis, Investigation Writing- Original draft preparation, Writing – Review & Editing, Visualization, Supervision. Hanin Karawani: Conceptualization, Investigation, Writing – Review & Editing, Samira Anderson: Conceptualization, Methodology, Software, Formal analysis, Writing – Review & Editing, Visualization, Project administration, Funding acquisition

CRediT authorship contribution statement

Abigail Anne Poe: Writing – original draft, Methodology, Investigation, Formal analysis. Hanin Karawani: Writing – review & editing, Supervision, Investigation. Samira Anderson: Writing – review & editing, Supervision, Project administration, Methodology, Investigation, Funding acquisition, Formal analysis, Conceptualization.

Acknowledgements

The authors wish to thank Lindsey Roque, Caitlin Le, Alanna Schloss, and Logan Fraser for their help with data collection and analysis. The authors also wish to thank Sandra Gordon-Salant for providing the word stimuli used in the study.

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