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

“…While FFR currents have been demonstrated in earlier work ( Steinschneider et al, 1999 , 2003 ) for steady fundamental frequencies <100 Hz, here, we show that cortical FFR currents show phase-locked activity as high as 150 Hz and follow the Mandarin pitch contours. These FFR currents could have partially contributed to the cortical FFR components found in earlier studies using non-invasive assays ( Coffey et al, 2016 , 2021 ; Bidelman, 2018 ; Gorina-Careta et al, 2021 ) and invasive assays ( Behroozmand et al, 2016 ; Guo et al, 2021 ). However, it should be noted that the nonlaminar assays (both non-invasive and invasive) could very well pick up both presynaptic and postsynaptic currents that effectively constitute the cortical FFRs ( Fig.…”

“…Research spanning 3 decades has richly characterized the properties of subcortical FFRs ( Chandrasekaran and Kraus, 2010 ; Skoe and Kraus, 2010 ; 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 (intracranial, scalp) platform to study cortical FFRs and their contribution to the scalp-recorded FFRs.…”

“…Furthermore, the periodicity code of pitch is thought to be transformed into a rate or rate-place code in the upper brainstem based on FFR studies ( 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 , 2021 ; Hartmann and Weisz, 2019 ; Gorina-Careta et al, 2021 ). However, non-invasive MEG and EEG studies require inferences based on distributed source-modeling approaches that are relatively less sensitive to deep brain sources.…”

Connectomics of Human Electrophysiology

“…Indeed, cortical and subcortical (e.g., thalamic) hubs of the brain's small-world architecture may act as dynamical relays and enable such phase-correction capability in recurrent brain networks (Bassett and Bullmore, 2006;Vicente et al, 2008). In dynamical terms, the compensation of phase delays or instantaneous frequency adjustments between distant nodes occur over a transition period, while feedback signals "catch up" with signal input changes in closed-loop neural circuits (Coffey et al, 2021;Cottereau et al, 2011). From an ecological perspective, the minimization of such transition periods may be critical to behaviour e.g., when fast motor action is required to avoid a looming object or to register fast-changing speech stimuli in a conversation (Donhauser and Baillet, 2020).…”

Resonance as a Design Strategy for AI and Social Robots

“…Although the term “resonance” is often intended as a metaphor to describe an interaction, in many cases physical resonance may also be a mechanism underlying the interaction. For instance, people metaphorically “resonate with music” but the brain also physically resonates with music: the actual frequencies of sound and rhythm can be observed in the frequencies of electrical activity in the brain (Coffey et al, 2019 , 2021 ; Kaneshiro et al, 2021 ; Pandey et al, 2021 ). Or, consider the common expression “syncing up” to describe a meeting.…”