Aging affects neural precision of speech encoding

Abstract

Older adults frequently report they can hear what is said but cannot understand the meaning, especially in noise. This difficulty may arise from the inability to process rapidly changing elements of speech. Aging is accompanied by a general slowing of neural processing and decreased neural inhibition, both of which likely interfere with temporal processing in auditory and other sensory domains. Age-related reductions in inhibitory neurotransmitter levels and delayed neural recovery can contribute to decreases in the temporal precision of the auditory system. Decreased precision may lead to neural timing delays, reductions in neural response magnitude, and a disadvantage in processing the rapid acoustic changes in speech. The auditory brainstem response (ABR), a scalp-recorded electrical potential, is known for its ability to capture precise neural synchrony within subcortical auditory nuclei; therefore, we hypothesized that a loss of temporal precision results in subcortical timing delays and decreases in response consistency and magnitude. To assess this hypothesis, we recorded ABRs to the speech syllable /da/ in normal hearing younger (18-30 years old) and older (60-67 years old) adult humans. Older adults had delayed ABRs, especially in response to the rapidly changing formant transition, and greater response variability. We also found that older adults had decreased phase locking and smaller response magnitudes than younger adults. Together, our results support the theory that older adults have a loss of temporal precision in the subcortical encoding of sound, which may account, at least in part, for their difficulties with speech perception.

Figure 1.

Average hearing thresholds are plotted from 125 to 8000 Hz for younger (red circles) and older (black diamonds) adults, with error bars indicating ±1 SE. Hearing thresholds between the two groups are equivalent, except at 4000 and 8000 Hz (both p < 0.001). Inset, average click-evoked waveforms for younger and older adults. Latencies are equivalent for waves I and III; there is a trending difference for wave V (p = 0.083).

Figure 2.

A, B, Stimulus waveform (A) and spectrogram (B) for the speech syllable /da/. C, Average brainstem responses to /da/ in the younger (red) and older (black) adults. The prestimulus and response regions are labeled with respect to the onset, formant transition, and steady-state vowel of the stimulus.

Figure 3.

Neural delays in the aging population. Older adults show a shift in neural response timing for both the onset and transition but not for the steady state. To facilitate visualization of the data, the peak latencies are normalized. Normalization was accomplished by subtracting the expected response timing, based on stimulus characteristics and neural lag, from the actual response latency. Expected latencies were 9 ms for the onset and 33, 43, 53, 63, etc., until 163 ms for peaks during the transition and steady state. This resulted in a normalized value (milliseconds), with 0 indicating that peak occurred at its expected latency. *p < 0.05, **p < 0.01, ***p < 0.001. Error bars represent ±1 SE.

Figure 4.

Phase locking factor. Top, younger adults. Bottom, older adults. Stronger phase-locking power is seen in younger adults, from the fundamental frequency through the upper harmonics and throughout the entire response.

Figure 5.

A, Bar graphs demonstrating significant between-group differences in RMS amplitude across stimulus time ranges. The older adults have higher prestimulus activity as measured by RMS amplitude, yet the younger adults have higher RMS response amplitudes. B, C, Fast Fourier transforms calculated over the entire response. B, Group average responses to added polarities in younger (red) versus older (black) adults. Greater magnitudes were noted in the 20 Hz bins surrounding lower frequencies, which contribute to pitch perception [fundamental frequency (F₀), second harmonic (H₂), and third harmonic (H₃)]. C, Group average responses to subtracted polarities in younger (red) versus older (black) adults. Greater magnitudes for younger adults were noted over the entire response but specifically for H₄–H₇ (the range encompassing the first formant). *p < 0.05, **p < 0.01. Dotted lines and error bars represent ±1 SE.