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Phase Entrainment of Brain Oscillations Causally Modulates Neural Responses to Intelligible Speech.

ABSTRACT: Due to their periodic nature, neural oscillations might represent an optimal "tool" for the processing of rhythmic stimulus input [1-3]. Indeed, the alignment of neural oscillations to a rhythmic stimulus, often termed phase entrainment, has been repeatedly demonstrated [4-7]. Phase entrainment is central to current theories of speech processing [8-10] and has been associated with successful speech comprehension [11-17]. However, typical manipulations that reduce speech intelligibility (e.g., addition of noise and time reversal [11, 12, 14, 16, 17]) could destroy critical acoustic cues for entrainment (such as "acoustic edges" [7]). Hence, the association between phase entrainment and speech intelligibility might only be "epiphenomenal"; i.e., both decline due to the same manipulation, without any causal link between the two [18]. Here, we use transcranial alternating current stimulation (tACS [19]) to manipulate the phase lag between neural oscillations and speech rhythm while measuring neural responses to intelligible and unintelligible vocoded stimuli with sparse fMRI. We found that this manipulation significantly modulates the BOLD response to intelligible speech in the superior temporal gyrus, and the strength of BOLD modulation is correlated with a phasic modulation of performance in a behavioral task. Importantly, these findings are absent for unintelligible speech and during sham stimulation; we thus demonstrate that phase entrainment has a specific, causal influence on neural responses to intelligible speech. Our results not only provide an important step toward understanding the neural foundation of human abilities at speech comprehension but also suggest new methods for enhancing speech perception that can be explored in the future.

SUBMITTER: Zoefel B

PROVIDER: S-EPMC5807089 | biostudies-literature | 2018 Feb

REPOSITORIES: biostudies-literature

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Phase Entrainment of Brain Oscillations Causally Modulates Neural Responses to Intelligible Speech.

Zoefel Benedikt B Archer-Boyd Alan A Davis Matthew H MH

Current biology : CB 20180118 3

Due to their periodic nature, neural oscillations might represent an optimal "tool" for the processing of rhythmic stimulus input [1-3]. Indeed, the alignment of neural oscillations to a rhythmic stimulus, often termed phase entrainment, has been repeatedly demonstrated [4-7]. Phase entrainment is central to current theories of speech processing [8-10] and has been associated with successful speech comprehension [11-17]. However, typical manipulations that reduce speech intelligibility (e.g., ad ...[more]

PMID: 29358073

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Project description:OBJECTIVE:Optogenetic modulation of neural activity is a ubiquitous tool for basic investigation of brain circuits. While the majority of optogenetic paradigms rely on short light pulses to evoke synchronized activity of optically sensitized cells, many neurobiological processes are associated with slow local field potential (LFP) oscillations. Therefore, we developed a hybrid fiber probe capable of simultaneous electrophysiological recording and optical stimulation and used it to investigate the utility of sinusoidal light stimulation for evoking oscillatory neural activity in vivo across a broad frequency range. APPROACH:We fabricated hybrid fiber probes comprising a hollow cylindrical array of 9 electrodes and a flexible optical waveguide integrated within the core. We implanted these probes in the hippocampus of transgenic Thy1-ChR2-YFP mice that broadly express the blue-light sensitive cation channel channelrhodopsin 2 (ChR2) in excitatory neurons across the brain. The effects of the sinusoidal light stimulation were characterized and contrasted with those corresponding to pulsed stimulation in the frequency range of physiological LFP rhythms (3-128 Hz). MAIN RESULTS:Within hybrid probes, metal electrode surfaces were vertically aligned with the waveguide tip, which minimized optical stimulation artifacts in neurophysiological recordings. Sinusoidal stimulation resulted in reliable and coherent entrainment of LFP oscillations up to 70 Hz, the cutoff frequency of ChR2, with response amplitudes inversely scaling with the stimulation frequencies. Effectiveness of the stimulation was maintained for two months following implantation. SIGNIFICANCE:Alternative stimulation patterns complementing existing pulsed protocols, in particular sinusoidal light stimulation, are a prerequisite for investigating the physiological mechanisms underlying brain rhythms. So far, studies applying sinusoidal stimulation in vivo were limited to single stimulation frequencies. We show the feasibility of sinusoidal stimulation in vivo to induce coherent LFP oscillations across the entire frequency spectrum supported by the gating dynamics of ChR2 and introduce a hybrid fiber probe tailored to continuous light stimulation.

Project description:Highlights • Children with and without dyslexia showed consistent phase entrainment.• Dyslexic children had significantly reduced delta band phase consistency.• Dyslexic children had a different preferred phase in delta compared to controls.• The dyslexic brain showed faster pre-stimulus delta band angular velocity. According to the sensory-neural Temporal Sampling theory of developmental dyslexia, neural sampling of auditory information at slow rates (<10 Hz, related to speech rhythm) is atypical in dyslexic individuals, particularly in the delta band (0.5–4 Hz). Here we examine the underlying neural mechanisms related to atypical sampling using a simple repetitive speech paradigm. Fifty-one children (21 control children [15M, 6F] and 30 children with dyslexia [16M, 14F]) aged 9 years with or without developmental dyslexia watched and listened as a ‘talking head’ repeated the syllable “ba” every 500 ms, while EEG was recorded. Occasionally a syllable was “out of time”, with a temporal delay calibrated individually and adaptively for each child so that it was detected around 79.4% of the time by a button press. Phase consistency in the delta (rate of stimulus delivery), theta (speech-related) and alpha (control) bands was evaluated for each child and each group. Significant phase consistency was found for both groups in the delta and theta bands, demonstrating neural entrainment, but not the alpha band. However, the children with dyslexia showed a different preferred phase and significantly reduced phase consistency compared to control children, in the delta band only. Analysis of pre- and post-stimulus angular velocity of group preferred phases revealed that the children in the dyslexic group showed an atypical response in the delta band only. The delta-band pre-stimulus angular velocity (−130 ms to 0 ms) for the dyslexic group appeared to be significantly faster compared to the control group. It is concluded that neural responding to simple beat-based stimuli may provide a unique neural marker of developmental dyslexia. The automatic nature of this neural response may enable new tools for diagnosis, as well as opening new avenues for remediation.

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Phase Entrainment of Brain Oscillations Causally Modulates Neural Responses to Intelligible Speech.

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Phase Entrainment of Brain Oscillations Causally Modulates Neural Responses to Intelligible Speech.

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