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Phase-amplitude coupling between theta and gamma oscillations adapts to speech rate.

ABSTRACT: Low- and high-frequency cortical oscillations play an important role in speech processing. Low-frequency neural oscillations in the delta (<4 Hz) and theta (4-8 Hz) bands entrain to the prosodic and syllabic rates of speech, respectively. Theta band neural oscillations modulate high-frequency neural oscillations in the gamma band (28-40 Hz), which have been hypothesized to be crucial for processing phonemes in natural speech. Since speech rate is known to vary considerably, both between and within talkers, it has yet to be determined whether this nested gamma response reflects an externally induced rhythm sensitive to the rate of the fine-grained structure of the input or a speech rate-independent endogenous response. Here, we recorded magnetoencephalography responses from participants listening to a speech delivered at different rates: decelerated, normal, and accelerated. We found that the phase of theta band oscillations in left and right auditory regions adjusts to speech rate variations. Importantly, we showed that the peak of the gamma response-coupled to the phase of theta-follows the speech rate. This indicates that gamma activity in auditory regions synchronizes with the fine-grain properties of speech, possibly reflecting detailed acoustic analysis of the input.

SUBMITTER: Lizarazu M

PROVIDER: S-EPMC6850406 | biostudies-literature | 2019 Oct

REPOSITORIES: biostudies-literature

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Phase-amplitude coupling between theta and gamma oscillations adapts to speech rate.

Lizarazu Mikel M Lallier Marie M Molinaro Nicola N

Annals of the New York Academy of Sciences 20190424 1

Low- and high-frequency cortical oscillations play an important role in speech processing. Low-frequency neural oscillations in the delta (<4 Hz) and theta (4-8 Hz) bands entrain to the prosodic and syllabic rates of speech, respectively. Theta band neural oscillations modulate high-frequency neural oscillations in the gamma band (28-40 Hz), which have been hypothesized to be crucial for processing phonemes in natural speech. Since speech rate is known to vary considerably, both between and with ...[more]

PMID: 31020680

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Project description:BackgroundHow oscillatory brain rhythms alone, or in combination, influence cortical information processing to support learning has yet to be fully established. Local field potential and multi-unit neuronal activity recordings were made from 64-electrode arrays in the inferotemporal cortex of conscious sheep during and after visual discrimination learning of face or object pairs. A neural network model has been developed to simulate and aid functional interpretation of learning-evoked changes.ResultsFollowing learning the amplitude of theta (4-8 Hz), but not gamma (30-70 Hz) oscillations was increased, as was the ratio of theta to gamma. Over 75% of electrodes showed significant coupling between theta phase and gamma amplitude (theta-nested gamma). The strength of this coupling was also increased following learning and this was not simply a consequence of increased theta amplitude. Actual discrimination performance was significantly correlated with theta and theta-gamma coupling changes. Neuronal activity was phase-locked with theta but learning had no effect on firing rates or the magnitude or latencies of visual evoked potentials during stimuli. The neural network model developed showed that a combination of fast and slow inhibitory interneurons could generate theta-nested gamma. By increasing N-methyl-D-aspartate receptor sensitivity in the model similar changes were produced as in inferotemporal cortex after learning. The model showed that these changes could potentiate the firing of downstream neurons by a temporal desynchronization of excitatory neuron output without increasing the firing frequencies of the latter. This desynchronization effect was confirmed in IT neuronal activity following learning and its magnitude was correlated with discrimination performance.ConclusionsFace discrimination learning produces significant increases in both theta amplitude and the strength of theta-gamma coupling in the inferotemporal cortex which are correlated with behavioral performance. A network model which can reproduce these changes suggests that a key function of such learning-evoked alterations in theta and theta-nested gamma activity may be increased temporal desynchronization in neuronal firing leading to optimal timing of inputs to downstream neural networks potentiating their responses. In this way learning can produce potentiation in neural networks simply through altering the temporal pattern of their inputs.

Project description:Neuronal oscillations support cognitive processing. Modern views suggest that neuronal oscillations do not only reflect coordinated activity in spatially distributed networks, but also that there is interaction between the oscillations at different frequencies. For example, invasive recordings in animals and humans have found that the amplitude of fast oscillations (>40 Hz) occur non-uniformly within the phase of slower oscillations, forming the so-called cross-frequency coupling (CFC). However, the CFC patterns might be influenced by features in the signal that do not relate to underlying physiological interactions. For example, CFC estimates may be sensitive to spectral correlations due to non-sinusoidal properties of the alpha band wave morphology. To investigate this issue, we performed CFC analysis using experimental and synthetic data. The former consisted in a double-blind magnetoencephalography pharmacological study in which participants received either placebo, 0.5 or 1.5 mg of lorazepam (LZP; GABAergic enhancer) in different experimental sessions. By recording oscillatory brain activity with during rest and working memory (WM), we were able to demonstrate that posterior alpha (8-12 Hz) phase was coupled to beta-low gamma band (20-45 Hz) amplitude envelope during all sessions. Importantly, bicoherence values around the harmonics of the alpha frequency were similar both in magnitude and topographic distribution to the cross-frequency coherence (CFCoh) values observed in the alpha-phase to beta-low gamma coupling. In addition, despite the large CFCoh we found no significant cross-frequency directionality (CFD). Critically, simulations demonstrated that a sizable part of our empirical CFCoh between alpha and beta-low gamma coupling and the lack of CFD could be explained by two-three harmonics aligned in zero phase-lag produced by the physiologically characteristic alpha asymmetry in the amplitude of the peaks relative to the troughs. Furthermore, we showed that periodic signals whose waveform deviate from pure sine waves produce non-zero CFCoh with predictable CFD. Our results reveal the important role of the non-sinusoidal wave morphology on state of the art CFC metrics and we recommend caution with strong physiological interpretations of CFC and suggest basic data quality checks to enhance the mechanistic understanding of CFC.

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Phase-amplitude coupling between theta and gamma oscillations adapts to speech rate.

Publications

Phase-amplitude coupling between theta and gamma oscillations adapts to speech rate.

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