Frontal Top-Down Signals Increase Coupling of Auditory Low-Frequency Oscillations to Continuous Speech in Human Listeners

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 [1Arnal L.H. Giraud A.L. Cortical oscillations and sensory predictions.Trends Cogn. Sci. 2012; 16: 390-398Abstract Full Text Full Text PDF PubMed Scopus (593) Google Scholar, 2Engel A.K. Fries P. Singer W. Dynamic predictions: oscillations and synchrony in top-down processing.Nat. Rev. Neurosci. 2001; 2: 704-716Crossref PubMed Scopus (2451) Google Scholar]. Quasi-rhythmic components in speech are known to entrain low-frequency oscillations in auditory areas [3Giraud A.L. Poeppel D. Cortical oscillations and speech processing: emerging computational principles and operations.Nat. Neurosci. 2012; 15: 511-517Crossref PubMed Scopus (1017) Google Scholar, 4Gross J. Hoogenboom N. Thut G. Schyns P. Panzeri S. Belin P. Garrod S. Speech rhythms and multiplexed oscillatory sensory coding in the human brain.PLoS Biol. 2013; 11: e1001752Crossref PubMed Scopus (326) Google Scholar], and this entrainment increases with intelligibility [5Peelle J.E. Gross J. Davis M.H. Phase-locked responses to speech in human auditory cortex are enhanced during comprehension.Cereb. Cortex. 2013; 23: 1378-1387Crossref PubMed Scopus (309) Google Scholar]. 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.