Oscillatory entrainment of the Frequency Following Response in auditory cortical and subcortical structures

Abstract

There is much debate about the existence and function of neural oscillatory entrainment mechanisms in the auditory system. The frequency-following response (FFR) is an index of neural periodicity encoding that can provide a vehicle to study entrainment in frequency ranges relevant to speech and music processing. Criteria for entrainment include the presence of post-stimulus oscillations and phase alignment between stimulus and endogenous activity. To test the hypothesis of entrainment, in experiment 1 we collected FFR data to a repeated syllable using magneto- (MEG) and electroencephalography in 20 healthy adults. We observed significant oscillatory activity after stimulus offset in auditory cortex and subcortical auditory nuclei, consistent with entrainment. In these structures the FFR fundamental frequency converged from a lower value over 100 ms to the stimulus frequency, consistent with phase alignment, and diverged to a lower value after offset, consistent with relaxation to a preferred frequency. In experiment 2, we tested how transitions between stimulus frequencies affected the MEG-FFR to a train of pure-tone pairs in 30 adults. We found that the FFR was affected by the frequency of the preceding tone for up to 40 ms at subcortical levels, and even longer durations at cortical levels. Our results suggest that oscillatory entrainment may be an integral part of periodic sound representation throughout the auditory neuraxis. The functional role of this mechanism is unknown, but it could serve as a fine-scale temporal predictor for frequency information, enhancing stability and reducing susceptibility to degradation that could be useful in real-life noisy environments.

Frequency-Following Responses to Speech Sounds Are Highly Conserved across Species and Contain Cortical Contributions

“…Research spanning three decades has richly characterized the properties of subcortical FFRs (Chandrasekaran and Kraus, 2010a;Skoe and Kraus, 2010a;Krizman and Kraus, 2019;Coffey et al, 2021), but open questions remain with respect to characteristics of the cortical FFR sources and their contribution to the scalp recorded FFRs. Our study establishes a cross-species (human, macaque, GP) and cross-level (intra-cranial, scalp) platform to study cortical FFRs and their contribution to the scalp-recorded FFRs.…”

“…Furthermore, periodicity code of pitch is thought to be transformed into a rate or rate-place code in the upper brainstem (Plack et al, 2014). Recent studies using magnetoencephalography (MEG) and EEG have challenged these accounts and shown substantial cortical contributions to the scalp FFRs, with a distinct rightward cortical asymmetry (Coffey et al, 2016(Coffey et al, , 2021Hartmann and Weisz, 2019;Gorina-Careta et al, 2021). However, non-invasive MEG and EEG studies require inferences based on distributed source modelling approaches which are relatively less sensitive to deep brain sources.…”

Deconstructing the Cortical Sources of Frequency Following Responses to Speech: A Cross-species Approach

“…For more than three decades, the inferior colliculus and the cochlear nucleus were considered the primary neural sources of the FFRs (5,10,11,(35)(36)(37). Emerging research demonstrates a robust cortical contribution to the scalprecorded FFRs (12,(38)(39)(40)(41). The neural dynamics and other response properties of the putative cortical ensembles contributing to the FFRs are poorly understood and will be the main focus of the current study.…”

“…The copyright holder for this preprint (which this version posted May 18, 2021. ; https://doi.org/10.1101/2021.05.17.444462 doi: bioRxiv preprint using magnetoencephalography (MEG) have challenged these accounts and shown strong cortical contributions to the scalp FFRs, with a distinct rightward cortical asymmetry (38)(39)(40). However, MEG studies require inferences based on distributional source modelling approaches which are relatively less sensitive to deep brain sources.…”

“…Furthermore, periodicity code of pitch is thought to be transformed into a rate or rate-place code in the upper brainstem (Plack et al, 2014). Recent studies using magnetoencephalography (MEG) and EEG have challenged these accounts and shown substantial cortical contributions to the scalp FFRs, with a distinct rightward cortical asymmetry (Coffey et al, 2016(Coffey et al, , 2021Hartmann and Weisz, 2019;Gorina-Careta et al, 2021). However, noninvasive MEG and EEG studies require inferences based on distributed source modelling approaches which are relatively less sensitive to deep brain sources.…”