Frontal top-down signals increase coupling of auditory low-frequency oscillations to continuous speech in human listeners

Park, H. , Ince, R. A.A., Schyns, P. G., Thut, G. and Gross, J. (2015) Frontal top-down signals increase coupling of auditory low-frequency oscillations to continuous speech in human listeners. Current Biology, 25(12), pp. 1649-1653. (doi:10.1016/j.cub.2015.04.049) (PMID:26028433) (PMCID:PMC4503802)

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Abstract

Humans show a remarkable ability to understand continuous speech even under adverse listening conditions. This ability critically relies on dynamically updated predictions of incoming sensory information, but exactly how top-down predictions improve speech processing is still unclear. Brain oscillations are a likely mechanism for these top-down predictions [1 and 2]. Quasi-rhythmic components in speech are known to entrain low-frequency oscillations in auditory areas [3 and 4], and this entrainment increases with intelligibility [5]. We hypothesize that top-down signals from frontal brain areas causally modulate the phase of brain oscillations in auditory cortex. We use magnetoencephalography (MEG) to monitor brain oscillations in 22 participants during continuous speech perception. We characterize prominent spectral components of speech-brain coupling in auditory cortex and use causal connectivity analysis (transfer entropy) to identify the top-down signals driving this coupling more strongly during intelligible speech than during unintelligible speech. We report three main findings. First, frontal and motor cortices significantly modulate the phase of speech-coupled low-frequency oscillations in auditory cortex, and this effect depends on intelligibility of speech. Second, top-down signals are significantly stronger for left auditory cortex than for right auditory cortex. Third, speech-auditory cortex coupling is enhanced as a function of stronger top-down signals. Together, our results suggest that low-frequency brain oscillations play a role in implementing predictive top-down control during continuous speech perception and that top-down control is largely directed at left auditory cortex. This suggests a close relationship between (left-lateralized) speech production areas and the implementation of top-down control in continuous speech perception.

Item Type:Articles
Status:Published
Refereed:Yes
Glasgow Author(s) Enlighten ID:Schyns, Professor Philippe and Thut, Professor Gregor and Park, Dr Hyojin and Ince, Dr Robin and Gross, Professor Joachim
Authors: Park, H., Ince, R. A.A., Schyns, P. G., Thut, G., and Gross, J.
College/School:College of Medical Veterinary and Life Sciences > Institute of Neuroscience and Psychology
Journal Name:Current Biology
Publisher:Elsevier
ISSN:0960-9822
ISSN (Online):1879-0445
Copyright Holders:Copyright © 2015 The Authors
First Published:First published in Current Biology 25(12):1649-1653
Publisher Policy:Reproduced under a Creative Commons License

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Project CodeAward NoProject NamePrincipal InvestigatorFunder's NameFunder RefLead Dept
597051Natural and modulated neural communication: State-dependent decoding and driving of human Brain Oscillations.Joachim GrossWellcome Trust (WELLCOME)098433/Z/12/ZINP - CENTRE FOR COGNITIVE NEUROIMAGING
597911Natural and modulated neural communication: State-dependent decoding and driving of human Brain OscillationsGregor ThutWellcome Trust (WELLCOME)098434/Z/12/ZINP - CENTRE FOR COGNITIVE NEUROIMAGING