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Concurrent temporal channels for auditory processing: Oscillatory neural entrainment reveals segregation of function at different scales.

ABSTRACT: Natural sounds convey perceptually relevant information over multiple timescales, and the necessary extraction of multi-timescale information requires the auditory system to work over distinct ranges. The simplest hypothesis suggests that temporal modulations are encoded in an equivalent manner within a reasonable intermediate range. We show that the human auditory system selectively and preferentially tracks acoustic dynamics concurrently at 2 timescales corresponding to the neurophysiological theta band (4-7 Hz) and gamma band ranges (31-45 Hz) but, contrary to expectation, not at the timescale corresponding to alpha (8-12 Hz), which has also been found to be related to auditory perception. Listeners heard synthetic acoustic stimuli with temporally modulated structures at 3 timescales (approximately 190-, approximately 100-, and approximately 30-ms modulation periods) and identified the stimuli while undergoing magnetoencephalography recording. There was strong intertrial phase coherence in the theta band for stimuli of all modulation rates and in the gamma band for stimuli with corresponding modulation rates. The alpha band did not respond in a similar manner. Classification analyses also revealed that oscillatory phase reliably tracked temporal dynamics but not equivalently across rates. Finally, mutual information analyses quantifying the relation between phase and cochlear-scaled correlations also showed preferential processing in 2 distinct regimes, with the alpha range again yielding different patterns. The results support the hypothesis that the human auditory system employs (at least) a 2-timescale processing mode, in which lower and higher perceptual sampling scales are segregated by an intermediate temporal regime in the alpha band that likely reflects different underlying computations.

SUBMITTER: Teng X

PROVIDER: S-EPMC5667736 | biostudies-literature | 2017 Nov

REPOSITORIES: biostudies-literature

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Concurrent temporal channels for auditory processing: Oscillatory neural entrainment reveals segregation of function at different scales.

Teng Xiangbin X Tian Xing X Rowland Jess J Poeppel David D

PLoS biology 20171102 11

Natural sounds convey perceptually relevant information over multiple timescales, and the necessary extraction of multi-timescale information requires the auditory system to work over distinct ranges. The simplest hypothesis suggests that temporal modulations are encoded in an equivalent manner within a reasonable intermediate range. We show that the human auditory system selectively and preferentially tracks acoustic dynamics concurrently at 2 timescales corresponding to the neurophysiological ...[more]

PMID: 29095816

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Project description: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.

Dataset Information

Concurrent temporal channels for auditory processing: Oscillatory neural entrainment reveals segregation of function at different scales.

Publications

Concurrent temporal channels for auditory processing: Oscillatory neural entrainment reveals segregation of function at different scales.

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