Cortical-brainstem interplay during speech perception in older adults with and without hearing loss

Lai, Jesyin; Alain, Claude; Bidelman, Gavin M.

doi:10.3389/fnins.2023.1075368

Cited by 6 publications

(9 citation statements)

References 95 publications

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“…Critically, the F0 (indeed all spectral cues) in our stimuli exceeded 250 Hz, which is substantially higher than the phase-locking limits of cortical neurons observed in any animal or human studies using either intracranial or far-field electrophysiological methods (Joris et al 2004;Brugge et al 2009 , showing that speech-FFRs represent categorical information of the speech signal, presumably due to influence of top-down projections to midbrain. The corticofugal influences on FFR seen here are consistent with other studies suggesting that these modulations are strongest at F0, though for unknown reasons (Yellamsetty and Bidelman 2019;Price and Bidelman 2021;Lai et al 2022;Carter and Bidelman 2023;Lai et al 2023). The change in F0 amplitude seen here must be driven by more than merely stimulus acoustics, likely due to top-down changes of FFR, as the acoustic F0 remained the same frequency and intensity across tokens.…”

Section: Category Representations Emerge Subcorticallysupporting

confidence: 89%

“…Critically, our stimuli require binaural integration to be categorically perceived; listeners cannot arrive at a phonetic label without integrating speech cues from the two ears. The fact FFRs mirrored the behavioral reports supports the notion that FFRs carry information about binaural integration and reflect listeners' online perceptual state (Lai et al 2022;Carter and Bidelman 2023;Lai et al 2023). Early binaural processing in the afferent auditory pathway begins in the superior olivary complex (Goldberg and Brown 1969), a site more caudal to the midbrain IC generators driving most of the FFR.…”

Section: Ffrs Reflect Binaural Integrationsupporting

confidence: 72%

“…Our data also reveal that FFRs represent binaurally integrated speech representations, reflecting a fused categorical percept. That binaural FFRs mirror listeners' endogenously generated, behavioral report further bolsters the notion that FFRs carry more than a neuro-acoustic code and instead reflect listeners' online perceptual state (Lai et al 2022;Carter and Bidelman 2023;Lai et al 2023).…”

Section: Discussionsupporting

confidence: 57%

“…Though cortex can contribute to FFRs under limited circumstances (Coffey, Herholz, et al 2016), speech-FFRs are dominantly generated by midbrain sources (i.e., inferior colliculus, IC) when recorded via EEG using high (> 150 Hz) fundamental frequency stimuli (Kiren et al 1994;López-Caballero et al 2020;Bidelman and Momtaz 2021;Gorina-Careta et al 2021;Price and Bidelman 2021). While the IC is likely too early along the processing hierarchy to show bottom-up, categorical organization de novo, top-down influences from cortex via the descending corticofugal system (Gao and Suga 1998) could modulate brainstem speech representations to produce categorical encoding effects as was recently observed in human FFRs (Price and Bidelman 2021;Lai et al 2022;Carter and Bidelman 2023;Lai et al 2023).…”

mentioning

confidence: 97%

“…This conflation of variables with behavior makes it difficult to isolate whether differences in neural activity truly index perception (endogenous coding) or are instead due to trivial acoustic mirroring (exogenous coding) (Carlyon 2004). Still, converging evidence suggests perceptual information may indeed drive changes in FFR when stimuli are well controlled and pit acoustic information orthogonal to the resulting percept-as afforded by categorization tasks (Price and Bidelman 2021;Lai et al 2022;Carter and Bidelman 2023;Lai et al 2023). Additionally, speech percepts that require binaural integration between the ears offer another viable test of perceptual correlates in FFR because information must be fused centrally to generate a category label.…”

mentioning

confidence: 99%

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Duplex perception reveals brainstem auditory representations are modulated by listeners’ ongoing percept for speech

Rizzi

Bidelman

2023

Preprint

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So-called duplex speech stimuli with perceptually ambiguous spectral cues to one ear and isolated low- vs. high-frequency third formant "chirp" to the opposite ear yield a coherent percept supporting their phonetic categorization. Critically, such dichotic sounds are only perceived categorically upon binaural integration. Here, we used frequency-following responses (FFRs), scalp-recorded potentials reflecting phase-locked subcortical activity, to investigate brainstem responses to fused speech percepts and to determine whether FFRs reflect binaurally integrated category-level representations. We recorded FFRs to diotic and dichotic stop-consonants (/da/, /ga/) that either did or did not require binaural fusion to properly label along with perceptually ambiguous sounds without clear phonetic identity. Behaviorally, listeners showed clear categorization of dichotic speech tokens confirming they were heard with a fused, phonetic percept. Neurally, we found FFRs were stronger for categorically perceived speech relative to category-ambiguous tokens but also differentiated phonetic categories for both diotically and dichotically presented speech sounds. Correlations between neural and behavioral data further showed FFR latency predicted the degree to which listeners labeled tokens as "da" vs. "ga". The presence of binaurally integrated, category-level information in FFRs suggests human brainstem processing reflects a surprisingly abstract level of the speech code typically circumscribed to much later cortical processing.

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Section: Category Representations Emerge Subcorticallysupporting

confidence: 89%

Section: Ffrs Reflect Binaural Integrationsupporting

confidence: 72%

Section: Discussionsupporting

confidence: 57%

mentioning

confidence: 97%

mentioning

confidence: 99%

See 3 more Smart Citations

Duplex perception reveals brainstem auditory representations are modulated by listeners’ ongoing percept for speech

Rizzi

Bidelman

2023

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

Duplex perception reveals brainstem auditory representations are modulated by listeners’ ongoing percept for speech

Rizzi

Bidelman

2023

Cerebral Cortex

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So-called duplex speech stimuli with perceptually ambiguous spectral cues to one ear and isolated low- versus high-frequency third formant “chirp” to the opposite ear yield a coherent percept supporting their phonetic categorization. Critically, such dichotic sounds are only perceived categorically upon binaural integration. Here, we used frequency-following responses (FFRs), scalp-recorded potentials reflecting phase-locked subcortical activity, to investigate brainstem responses to fused speech percepts and to determine whether FFRs reflect binaurally integrated category-level representations. We recorded FFRs to diotic and dichotic stop-consonants (/da/, /ga/) that either did or did not require binaural fusion to properly label along with perceptually ambiguous sounds without clear phonetic identity. Behaviorally, listeners showed clear categorization of dichotic speech tokens confirming they were heard with a fused, phonetic percept. Neurally, we found FFRs were stronger for categorically perceived speech relative to category-ambiguous tokens but also differentiated phonetic categories for both diotically and dichotically presented speech sounds. Correlations between neural and behavioral data further showed FFR latency predicted the degree to which listeners labeled tokens as “da” versus “ga.” The presence of binaurally integrated, category-level information in FFRs suggests human brainstem processing reflects a surprisingly abstract level of the speech code typically circumscribed to much later cortical processing.

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Aging impacts basic auditory and timing processes

Criscuolo,

Schwartze,

Bonetti

et al. 2024

Preprint

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Deterioration in the peripheral and central auditory systems is common in older adults and often leads to hearing and speech comprehension difficulties. Even when hearing remains intact, electrophysiological data of older adults frequently exhibit altered neural responses across the auditory pathway, reflected in variability in the phase alignment of neural activity to speech sound onsets. However, it remains unclear whether speech processing challenges in older adults stem from more fundamental deficits in auditory and timing processing. Here, we investigated the efficiency of aging individuals in encoding temporal regularities in acoustic sequences and their ability to predict future events. We recorded EEG in older and young individuals listening to simple isochronous tone sequences. A comprehensive analysis pipeline evaluated the amplitude, latency, and variability of event-related responses (ERPs) to each tone onset along the auditory sequences. Spectral parametrization and Inter-Trial Phase Coherence (ITPC) analyses assessed how participants encoded the temporal regularity in the acoustic environment. Our findings indicate that aging individuals exhibit altered temporal processing and reduced capacity to generate and utilize temporal predictions to time-lock and adaptively suppress neural responses to predictable and repeated tones in auditory sequences. Given that deteriorations in these basic timing capacities may affect other higher-order cognitive processes (e.g., attention, perception, and action), our results underscore the need for future research examining the link between timing abilities and general cognition across the lifespan.

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Cortical-brainstem interplay during speech perception in older adults with and without hearing loss

Cited by 6 publications

References 95 publications

Duplex perception reveals brainstem auditory representations are modulated by listeners’ ongoing percept for speech

Duplex perception reveals brainstem auditory representations are modulated by listeners’ ongoing percept for speech

Duplex perception reveals brainstem auditory representations are modulated by listeners’ ongoing percept for speech

Aging impacts basic auditory and timing processes

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