Human Frequency Following Response: Neural Representation of Envelope and Temporal Fine Structure in Listeners with Normal Hearing and Sensorineural Hearing Loss

Abstract

Objective: Listeners with sensorineural hearing loss (SNHL) typically experience reduced speech perception, which is not completely restored with amplification. This likely occurs because cochlear damage, in addition to elevating audiometric thresholds, alters the neural representation of speech transmitted to higher centers along the auditory neuroaxis. While the deleterious effects of SNHL on speech perception in humans have been well-documented using behavioral paradigms, our understanding of the neural correlates underlying these perceptual deficits remains limited. Using the scalp-recorded frequency following response (FFR), the authors examine the effects of SNHL and aging on subcortical neural representation of acoustic features important for pitch and speech perception, namely the periodicity envelope (F0) and temporal fine structure (TFS; formant structure), as reflected in the phase-locked neural activity generating the FFR.

Design: FFRs were obtained from 10 listeners with normal hearing (NH) and 9 listeners with mild-moderate SNHL in response to a steady-state English back vowel /u/ presented at multiple intensity levels. Use of multiple presentation levels facilitated comparisons at equal sound pressure level (SPL) and equal sensation level. In a second follow-up experiment to address the effect of age on envelope and TFS representation, FFRs were obtained from 25 NH and 19 listeners with mild to moderately severe SNHL to the same vowel stimulus presented at 80 dB SPL. Temporal waveforms, Fast Fourier Transform and spectrograms were used to evaluate the magnitude of the phase-locked activity at F0 (periodicity envelope) and F1 (TFS).

Results: Neural representation of both envelope (F0) and TFS (F1) at equal SPLs was stronger in NH listeners compared with listeners with SNHL. Also, comparison of neural representation of F0 and F1 across stimulus levels expressed in SPL and sensation level (accounting for audibility) revealed that level-related changes in F0 and F1 magnitude were different for listeners with SNHL compared with listeners with NH. Furthermore, the degradation in subcortical neural representation was observed to persist in listeners with SNHL even when the effects of age were controlled for.

Conclusions: Overall, our results suggest a relatively greater degradation in the neural representation of TFS compared with periodicity envelope in individuals with SNHL. This degraded neural representation of TFS in SNHL, as reflected in the brainstem FFR, may reflect a disruption in the temporal pattern of phase-locked neural activity arising from altered tonotopic maps and/or wider filters causing poor frequency selectivity in these listeners. Finally, while preliminary results indicate that the deleterious effects of SNHL may be greater than age-related degradation in subcortical neural representation, the lack of a balanced age-matched control group in this study does not permit us to completely rule out the effects of age on subcortical neural representation.

Figure 1

Average pure tone thresholds at audiometric test frequencies between 250 Hz–8000 Hz for the ear tested in NH (filled circles) and SNHL (open circles) listeners. Error bars represent standard errors.

Figure 2

Grand average waveforms for NH and SNHL (overlaid in panel A), and spectrograms (panel B: normal hearing and panel C: SNHL) plotted as a function of stimulus level in dB SPL for the FFR_ENV condition.

Figure 3

Mean F0 magnitudes (natural log transformed) plotted as a function of stimulus level (in dB SPL) for normal hearing (filled circles) and SNHL (open circles). Error bars represent standard errors.

Figure 4

Grand average waveforms for NH and SNHL (overlaid in panel A), and spectrograms (panel B: normal hearing and panel C: SNHL) plotted as a function of stimulus level in dB SL for the FFR_ENV condition.

Figure 5

Mean F0 magnitudes (natural log transformed) plotted as a function of stimulus level (in dB SL) for normal hearing (filled circles) and SNHL (open circles). Error bars represent standard errors.

Figure 6

Grand average waveforms for NH and SNHL (overlaid in panel A), and spectrograms (panel B: normal hearing and panel C: SNHL) plotted as a function of stimulus level (in dB SPL) for the FFR_TFS condition

Figure 7

Mean F1 magnitudes (natural log transformed) plotted as a function of stimulus level (in dB SPL) for normal hearing (filled circles) and SNHL (open circles). Error bars represent standard errors.

Figure 8

Grand average waveforms for NH and SNHL (overlaid in panel A), and spectrograms (panel B: normal hearing and panel C: SNHL) plotted as a function of stimulus level (in dB SL) for the FFR_TFS condition.

Figure 9

Mean F1 magnitudes (natural log transformed) plotted as a function of stimulus level (in dB SL) for normal hearing (filled circles) and SNHL (open circles). Error bars represent standard errors.