Dataset Information

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

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, 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.

SUBMITTER: Park H

PROVIDER: S-EPMC4503802 | biostudies-other | 2015 Jun

REPOSITORIES: biostudies-other

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

Park Hyojin H Ince Robin A A RA Schyns Philippe G PG Thut Gregor G Gross Joachim J

Current biology : CB 20150528 12

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, 2]. Quasi-rhythmic components in speech are known to entrain low-frequency oscillations in auditory areas [3, 4], and this entrainment in ...[more]

PMID: 26028433

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Project description:Alpha oscillations (8-12 Hz) are thought to inversely correlate with cortical excitability. Goal-oriented modulation of alpha has been studied extensively. In visual spatial attention, alpha over the region of visual cortex corresponding to the attended location decreases, signifying increased excitability to facilitate the processing of impending stimuli. In contrast, in retention of verbal working memory, alpha over visual cortex increases, signifying decreased excitability to gate out stimulus input to protect the information held online from sensory interference. According to the prevailing model, this goal-oriented biasing of sensory cortex is effected by top-down control signals from frontal and parietal cortices. The present study tests and substantiates this hypothesis by (a) identifying the signals that mediate the top-down biasing influence, (b) examining whether the cortical areas issuing these signals are task-specific or task-independent, and (c) establishing the possible mechanism of the biasing action. High-density human EEG data were recorded in two experimental paradigms: a trial-by-trial cued visual spatial attention task and a modified Sternberg working memory task. Applying Granger causality to both sensor-level and source-level data we report the following findings. In covert visual spatial attention, the regions exerting top-down control over visual activity are lateralized to the right hemisphere, with the dipoles located at the right frontal eye field (FEF) and the right inferior frontal gyrus (IFG) being the main sources of top-down influences. During retention of verbal working memory, the regions exerting top-down control over visual activity are lateralized to the left hemisphere, with the dipoles located at the left middle frontal gyrus (MFG) being the main source of top-down influences. In both experiments, top-down influences are mediated by alpha oscillations, and the biasing effect is likely achieved via an inhibition-disinhibition mechanism.

Project description:Neural processing along the ascending auditory pathway is often associated with a progressive reduction in characteristic processing rates. For instance, the well-known frequency-following response (FFR) of the auditory midbrain, as measured with electroencephalography (EEG), is dominated by frequencies from ?100?Hz to several hundred Hz, phase-locking to the acoustic stimulus at those frequencies. In contrast, cortical responses, whether measured by EEG or magnetoencephalography (MEG), are typically characterized by frequencies of a few Hz to a few tens of Hz, time-locking to acoustic envelope features. In this study we investigated a crossover case, cortically generated responses time-locked to continuous speech features at FFR-like rates. Using MEG, we analyzed responses in the high gamma range of 70-200?Hz to continuous speech using neural source-localized reverse correlation and the corresponding temporal response functions (TRFs). Continuous speech stimuli were presented to 40 subjects (17 younger, 23 older adults) with clinically normal hearing and their MEG responses were analyzed in the 70-200?Hz band. Consistent with the relative insensitivity of MEG to many subcortical structures, the spatiotemporal profile of these response components indicated a cortical origin with ?40?ms peak latency and a right hemisphere bias. TRF analysis was performed using two separate aspects of the speech stimuli: a) the 70-200?Hz carrier of the speech, and b) the 70-200?Hz temporal modulations in the spectral envelope of the speech stimulus. The response was dominantly driven by the envelope modulation, with a much weaker contribution from the carrier. Age-related differences were also analyzed to investigate a reversal previously seen along the ascending auditory pathway, whereby older listeners show weaker midbrain FFR responses than younger listeners, but, paradoxically, have stronger cortical low frequency responses. In contrast to both these earlier results, this study did not find clear age-related differences in high gamma cortical responses to continuous speech. Cortical responses at FFR-like frequencies shared some properties with midbrain responses at the same frequencies and with cortical responses at much lower frequencies.

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

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

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