Individual differences in the attentional modulation of the human auditory brainstem response to speech inform on speech-in-noise deficits

Abstract

People with normal hearing thresholds can nonetheless have difficulty with understanding speech in noisy backgrounds. The origins of such supra-threshold hearing deficits remain largely unclear. Previously we showed that the auditory brainstem response to running speech is modulated by selective attention, evidencing a subcortical mechanism that contributes to speech-in-noise comprehension. We observed, however, significant variation in the magnitude of the brainstem's attentional modulation between the different volunteers. Here we show that this variability relates to the ability of the subjects to understand speech in background noise. In particular, we assessed 43 young human volunteers with normal hearing thresholds for their speech-in-noise comprehension. We also recorded their auditory brainstem responses to running speech when selectively attending to one of two competing voices. To control for potential peripheral hearing deficits, and in particular for cochlear synaptopathy, we further assessed noise exposure, the temporal sensitivity threshold, the middle-ear muscle reflex, and the auditory-brainstem response to clicks in various levels of background noise. These tests did not show evidence for cochlear synaptopathy amongst the volunteers. Furthermore, we found that only the attentional modulation of the brainstem response to speech was significantly related to speech-in-noise comprehension. Our results therefore evidence an impact of topdown modulation of brainstem activity on the variability in speech-in-noise comprehension amongst the subjects.Understanding speech in noisy backgrounds such as other competing speakers is a challenging task at which humans excel 1,2 It requires the separation of different sound sources, selective attention to the target speaker, and the processing of degraded signals 3-5 Hearing impairment such as resulting from noise exposure often leads to an increase of hearing thresholds, a reduction in the information conveyed about a sound to the central auditory system, and thus to greater difficulty in understanding speech in noise 6-8 However, even listeners with normal hearing thresholds can have problems with understanding speech in noisy environments 9,10 .An extensive neural network of efferent fibers can feed information from the central auditory cortex back to the auditory brainstem and even to the cochlea 11,12 . Research on the role of these neural feedback loops for speech-in-noise listening has mostly focused on the medial olivocochlear reflex (MOCR), in which stimulation of the medial olivocochlear fibers that synapse on the outer hair cells in the cochlea reduces cochlear amplification across a wide frequency band 13 . Computational modelling as well as animal studies have shown that such reduced broad-band amplification can improve the signal-to-noise ratio of a transient signal embedded in background noise [14][15][16][17] . However, it remains debated whether the reduction of cochlear amplification through the MOCR contributes to better speech-in-noise comprehe...

Exposing distinct subcortical components of the auditory brainstem response evoked by continuous naturalistic speech

“…Indeed, a 50 Hz change in fundamental frequency yields a 24% reduction in the modelled auditory brainstem response that was derived as the complex cross-correlation with the fundamental frequency (Saiz-Alia and Reichenbach, 2020). The narrator differences exhibited in the present study may be larger than those in other studies with continuous speech (Forte et al, 2017; Maddox and Lee, 2018; Saiz-Alía et al, 2019) as a result of the different regressors. These response differences do not preclude using narrators with higher fundamental frequencies in future studies, but the time required for usable responses from each narrator must be considered when planning experiments, and caution taken when interpreting comparisons between conditions with differing narrators.…”

“…The responses to embedded chirps elicited waves with larger mean amplitude than those to our broadband peaky speech (~0.4 versus ~0.2 μV, respectively), although a similar proportion of subjects had identifiable waves and several other factors may contribute to amplitude differences. For example, higher click rates (e.g., Burkard et al, 1990; Burkard and Hecox, 1983; Chiappa et al, 1979; Don et al, 1977; Jiang et al, 2009) and higher fundamental frequencies (Maddox and Lee, 2018; Saiz-Alía et al, 2019; Saiz-Alia and Reichenbach, 2020) reduce the brainstem response amplitude, and dynamic changes in rate may create interactions across neural populations that lead to smaller amplitudes. Our stimuli kept the dynamic changes in pitch across all frequencies (instead of alternate octave bands of chirps and speech) and created impulses at every glottal pulse, with an average pitch of ~115 Hz and ~198 Hz for the male and female narrators respectively.…”

“…Although clicks also evoke responses with multiple component waves, current studies of synaptopathy show quite varied results with clicks and poor correlation with speech in noise (Bramhall et al, 2019;Prendergast et al, 2017). Obtaining click-like responses to stimuli with all of speech's spectrotemporal richness may provide a better connection to the specific neural underpinnings of speech encoding, similar to how the complex cross-correlation to a fundamental waveform can change based on the context of attention (Forte et al, 2017;Saiz-Alía et al, 2019).…”

Attention reinforces human corticofugal system to aid speech perception in noise

“…Some electrophysiological studies suggest attention enhances the robustness and temporal precision of speech FFRs (Forte et al, 2017;Galbraith et al, 2003;Hartmann and Weisz, 2019;Lehmann and Schonwiesner, 2014). Still, others demonstrate mixed (Holmes et al, 2018;Saiz-Alia et al, 2019) or even null attentionrelated FFR effects (Galbraith and Kane, 1993;Varghese et al, 2015). Brainstem responses are reliably recorded during sleep and sedation (Skoe and Kraus, 2010a) which bolsters long-held assumptions that subcortical processing is largely pre-attentive and automatic (Tzounopoulos and Kraus, 2009).…”

Automatic Recognition of Auditory Brainstem Response Characteristic Waveform Based on Bidirectional Long Short-Term Memory

“…Auditory brainstem response (ABR) is a global neural activity in the auditory brainstem centers evoked by acoustic stimulations. It can observe the functional status of the auditory nerve and lower auditory center and reflect the conduction ability of the brainstem auditory pathway ( 1 , 2 ). Given that patient's hearing impairment can be diagnosed without his active cooperation, ABR has become one of the routine methods for adult hearing recording ( 3 – 5 ).…”