SummaryHumans 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, 2]. Quasi-rhythmic components in speech are known to entrain low-frequency oscillations in auditory areas [3, 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.

During continuous speech, lip movements provide visual temporal signals that facilitate speech processing. Here, using MEG we directly investigated how these visual signals interact with rhythmic brain activity in participants listening to and seeing the speaker. First, we investigated coherence between oscillatory brain activity and speaker’s lip movements and demonstrated significant entrainment in visual cortex. We then used partial coherence to remove contributions of the coherent auditory speech signal from the lip-brain coherence. Comparing this synchronization between different attention conditions revealed that attending visual speech enhances the coherence between activity in visual cortex and the speaker’s lips. Further, we identified a significant partial coherence between left motor cortex and lip movements and this partial coherence directly predicted comprehension accuracy. Our results emphasize the importance of visually entrained and attention-modulated rhythmic brain activity for the enhancement of audiovisual speech processing.DOI: http://dx.doi.org/10.7554/eLife.14521.001

These findings indicate that patterns of metabolic connectivity of functional brain units depend on their regional locations. We propose that interregional correlation analysis of FDG-PET data offers a means of examining voxel-wise regional metabolic connectivity of the resting human brain.

Integration of multimodal sensory information is fundamental to many aspects of human behavior, but the neural mechanisms underlying these processes remain mysterious. For example, during face-to-face communication, we know that the brain integrates dynamic auditory and visual inputs, but we do not yet understand where and how such integration mechanisms support speech comprehension. Here, we quantify representational interactions between dynamic audio and visual speech signals and show that different brain regions exhibit different types of representational interaction. With a novel information theoretic measure, we found that theta (3–7 Hz) oscillations in the posterior superior temporal gyrus/sulcus (pSTG/S) represent auditory and visual inputs redundantly (i.e., represent common features of the two), whereas the same oscillations in left motor and inferior temporal cortex represent the inputs synergistically (i.e., the instantaneous relationship between audio and visual inputs is also represented). Importantly, redundant coding in the left pSTG/S and synergistic coding in the left motor cortex predict behavior—i.e., speech comprehension performance. Our findings therefore demonstrate that processes classically described as integration can have different statistical properties and may reflect distinct mechanisms that occur in different brain regions to support audiovisual speech comprehension.