Afferent-efferent connectivity between auditory brainstem and cortex accounts for poorer speech-in-noise comprehension in older adults

Bidelman, Gavin M.; Price, Caitlin N.; Shen, Dawei; Arnott, Stephen R.; Alain, Claude

doi:10.1101/568840

Cited by 15 publications

(54 citation statements)

References 98 publications

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“…2I). Critically, attention enhanced P2 (F1, 136 = 4.97, p = 0.03), confirming its role in active listening (Naatanen, 1975;Picton and Hillyard, 1974) and a biomarker of SIN perception (Bidelman et al, 2019). No other significant effects or interactions were found.3.3 Brainstem-cortical functional connectivity…”

Section: Cortical Erpsmentioning

confidence: 77%

“…Twenty young adults (age: 18-35 years, M = 24, SD = 3.4 years; 11 female) participated in the study. An a priori power analysis (t-test, 2-tailed,  = 0.05, power = 95%) revealed this sample was sufficient to detect similar sized effects (d = 0.84, 1.0) as in previous FFR/ERP SIN studies (Bidelman et al, 2019;GPower v3.1). All participants exhibited normal hearing thresholds ( 25 dB HL; 250-8000 Hz).…”

Section: Participantsmentioning

confidence: 84%

“…We recorded FFRs and ERPs simultaneously (Bidelman et al, 2013;Bidelman et al, 2019) during SIN-listening tasks designed to evaluate attentional effects on the brain's hierarchical encoding of speech. Three synthesized vowel tokens (e.g., /a/, /i/, /u/) were presented during the recording of EEGs.…”

Section: Speech Stimuli and Taskmentioning

confidence: 99%

“…Three synthesized vowel tokens (e.g., /a/, /i/, /u/) were presented during the recording of EEGs. We chose vowels as sustained periodic sounds optimally evoke FFRs and ERPs (Bidelman et al, 2019;Skoe and Kraus, 2010a). Each vowel was 100 ms with a common voice fundamental frequency (F0=150 Hz).…”

Section: Speech Stimuli and Taskmentioning

confidence: 99%

“…We measured functional connectivity between PAC and BS source waveforms using phase transfer entropy (PTE), a measure of nonlinear, directed (causal) signal dependency (Bidelman et al, 2018;Bidelman et al, 2019;Price et al, 2019). For details, see Lobier et al, 2014.…”

Section: Functional Connectivitymentioning

confidence: 99%

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Attention reinforces human corticofugal system to aid speech perception in noise

Price

Bidelman

2020

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Perceiving speech-in-noise (SIN) demands precise neural coding between brainstem and cortical levels of the hearing system. Attentional processes can then select and prioritize task-relevant cues over competing background noise for successful speech perception. In animal models, brainstem-cortical interplay is achieved via descending corticofugal projections from cortex that shape midbrain responses to behaviorally-relevant sounds. Attentional engagement of corticofugal feedback may assist SIN understanding but has never been confirmed and remains highly controversial in humans. To resolve these issues, we recorded source-level, anatomically constrained brainstem frequency-following responses (FFRs) and cortical event-related potentials (ERPs) to speech via high-density EEG while listeners performed rapid SIN identification tasks. We varied attention with active vs. passive listening scenarios whereas task difficulty was manipulated with additive noise interference. Active listening (but not arousal-control tasks) exaggerated both ERPs and FFRs, confirming attentional gain extends to lower subcortical levels of speech processing. We used functional connectivity to measure the directed strength of coupling between levels and characterize bottom-up vs. top-down (corticofugal) signaling within the auditory brainstem-cortical pathway. While attention strengthened connectivity bidirectionally, corticofugal transmission disengaged under passive (but not active) SIN listening. Our findings (i) show attention enhances neural transcription of speech even prior to cortex and (ii) establish a direct role of the human corticofugal feedback system as an aid to cocktail party speech perception.

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Section: Cortical Erpsmentioning

confidence: 77%

Section: Participantsmentioning

confidence: 84%

Section: Speech Stimuli and Taskmentioning

confidence: 99%

Section: Speech Stimuli and Taskmentioning

confidence: 99%

Section: Functional Connectivitymentioning

confidence: 99%

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Attention reinforces human corticofugal system to aid speech perception in noise

Price

Bidelman

2020

Preprint

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Age-related hearing loss increases full-brain connectivity while reversing directed signaling within the dorsal–ventral pathway for speech

et al. 2019

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Speech comprehension difficulties are ubiquitous to aging and hearing loss, particularly in noisy environments. Older adults' poorer speech-in-noise (SIN) comprehension has been related to abnormal neural representations within various nodes (regions) of the speech network, but how senescent changes in hearing alter the transmission of brain signals remains unspecified. We measured electroencephalograms in older adults with and without mild hearing loss during a SIN identification task. Using functional connectivity and graph-theoretic analyses, we show that hearing-impaired (HI) listeners have more extended (less integrated) communication pathways and less efficient information exchange among widespread brain regions (larger network eccentricity) than their normal-hearing (NH) peers. Parameter optimized support vector machine classifiers applied to EEG connectivity data showed hearing status could be decoded (> 85% accuracy) solely using network-level descriptions of brain activity, but classification was particularly robust using left hemisphere connections. Notably, we found a reversal in directed neural signaling in left hemisphere dependent on hearing status among specific connections within the dorsalventral speech pathways. NH listeners showed an overall net "bottom-up" signaling directed from auditory cortex (A1) to inferior frontal gyrus (IFG; Broca's area), whereas the HI group showed the reverse signal (i.e., "top-down" Broca's → A1). A similar flow reversal was noted between

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Multiple Cases of Auditory Neuropathy Illuminate the Importance of Subcortical Neural Synchrony for Speech-in-noise Recognition and the Frequency-following Response

et al. 2021

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Objectives: The role of subcortical synchrony in speech-in-noise (SIN) recognition and the frequency-following response (FFR) was examined in multiple listeners with auditory neuropathy. Although an absent FFR has been documented in one listener with idiopathic neuropathy who has severe difficulty recognizing SIN, several etiologies cause the neuropathy phenotype. Consequently, it is necessary to replicate absent FFRs and concomitant SIN difficulties in patients with multiple sources and clinical presentations of neuropathy to elucidate fully the importance of subcortical neural synchrony for the FFR and SIN recognition. Design: Case series. Three children with auditory neuropathy (two males with neuropathy attributed to hyperbilirubinemia, one female with a rare missense mutation in the OPA1 gene) were compared to age-matched controls with normal hearing (52 for electrophysiology and 48 for speech recognition testing). Tests included standard audiological evaluations, FFRs, and sentence recognition in noise. The three children with neuropathy had a range of clinical presentations, including moderate sensorineural hearing loss, use of a cochlear implant, and a rapid progressive hearing loss. Results: Children with neuropathy generally had good speech recognition in quiet but substantial difficulties in noise. These SIN difficulties were somewhat mitigated by a clear speaking style and presenting words in a high semantic context. In the children with neuropathy, FFRs were absent from all tested stimuli. In contrast, age-matched controls had reliable FFRs. Conclusion: Subcortical synchrony is subject to multiple forms of disruption but results in a consistent phenotype of an absent FFR and substantial difficulties recognizing SIN. These results support the hypothesis that subcortical synchrony is necessary for the FFR. Thus, in healthy listeners, the FFR may reflect subcortical neural processes important for SIN recognition.

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Afferent-efferent connectivity between auditory brainstem and cortex accounts for poorer speech-in-noise comprehension in older adults

Cited by 15 publications

References 98 publications

Attention reinforces human corticofugal system to aid speech perception in noise

Attention reinforces human corticofugal system to aid speech perception in noise

Age-related hearing loss increases full-brain connectivity while reversing directed signaling within the dorsal–ventral pathway for speech

Multiple Cases of Auditory Neuropathy Illuminate the Importance of Subcortical Neural Synchrony for Speech-in-noise Recognition and the Frequency-following Response

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