Neural Entrainment Meets Behavior: The Stability Index as a Neural Outcome Measure of Auditory-Motor Coupling

Abstract

Understanding rhythmic behavior in the context of coupled auditory and motor systems has been of interest to neurological rehabilitation, in particular, to facilitate walking. Recent work based on behavioral measures revealed an entrainment effect of auditory rhythms on motor rhythms. In this study, we propose a method to compute the neural component of such a process from an electroencephalographic (EEG) signal. A simple auditory-motor synchronization paradigm was used, where 28 healthy participants were instructed to synchronize their finger-tapping with a metronome. The computation of the neural outcome measure was carried out in two blocks. In the first block, we used Generalized Eigendecomposition (GED) to reduce the data dimensionality to the component which maximally entrained to the metronome frequency. The scalp topography pointed at brain activity over contralateral sensorimotor regions. In the second block, we computed instantaneous frequency from the analytic signal of the extracted component. This returned a time-varying measure of frequency fluctuations, whose standard deviation provided our “stability index” as a neural outcome measure of auditory-motor coupling. Finally, the proposed neural measure was validated by conducting a correlation analysis with a set of behavioral outcomes from the synchronization task: resultant vector length, relative phase angle, mean asynchrony, and tempo matching. Significant moderate negative correlations were found with the first three measures, suggesting that the stability index provided a quantifiable neural outcome measure of entrainment, with selectivity towards phase-correction mechanisms. We address further adoption of the proposed approach, especially with populations where sensorimotor abilities are compromised by an underlying pathological condition. The impact of using stability index can potentially be used as an outcome measure to assess rehabilitation protocols, and possibly provide further insight into neuropathological models of auditory-motor coupling.

Auditory Cue Effects on Gait-Phase-Dependent Electroencephalogram (EEG) Modulations during Overground and Treadmill Walking

“…This finding contradicts previous research suggesting heightened brain activity when processing auditory and sensorimotor-related information [ 28 , 42 ]. For instance, past studies have linked the left temporal cortex to responses to auditory cues, such as synchronizing finger-tapping with a metronome [ 43 ]. This brain area typically plays a role in receiving and interpreting auditory cues related to a desired walking speed.…”

Auditory attention measured by EEG in neurological populations: systematic review of literature and meta-analysis

“…Building on the theme of adaptation, we hereby address the recent development of methodologies designed to capture the dynamic nature of attending 7 , 82 . In particular, measuring variations in the frequency of oscillatory brain components attuned to the rhythmic stimulus has the potential for future fundamental research on the clinical populations investigated in the present work 83 , 84 . Among these developments, we point at event-related frequency adjustments (ERFAs) as a viable alternative to traditional ERPs paradigms, to investigate how different pathologies selectively impair oscillatory dynamics underlying auditory attention and sensorimotor synchronization (for details on the experimental paradigm, see 84 ).…”

Effects of Stimulus Rate and Periodicity on Auditory Cortical Entrainment to Continuous Sounds

“…Entrainment applies to a wide range of physiologically important behaviors including auditory–motor coupling ( Fujii and Schlaug, 2013 ; Herbst and Landau, 2016 ; Nozaradan et al, 2016 ; Moumdjian et al, 2018 ; Rosso et al, 2021 ) as well as speech ( Peelle and Davis, 2012 ) and music ( Fiveash et al, 2021 ) perception. For example, listeners must segment the continuous input speech signal into proper discrete units (i.e., syllables), which are then used as input for future decoding stages by auditory and nonauditory brain regions.…”