scholarly journals Sustained neural rhythms reveal endogenous oscillations supporting speech perception

PLoS Biology ◽  
2021 ◽  
Vol 19 (2) ◽  
pp. e3001142
Author(s):  
Sander van Bree ◽  
Ediz Sohoglu ◽  
Matthew H. Davis ◽  
Benedikt Zoefel
Keyword(s):  
Electrical Stimulation ◽  
Speech Perception ◽  
Oscillatory Activity ◽  
Neural Oscillations ◽  
Evoked Responses ◽  
Sustained Effects ◽  
Brain Responses ◽  
Underlying Principle ◽  
Transcranial Alternating Current Stimulation ◽  
Neural Entrainment

Rhythmic sensory or electrical stimulation will produce rhythmic brain responses. These rhythmic responses are often interpreted as endogenous neural oscillations aligned (or “entrained”) to the stimulus rhythm. However, stimulus-aligned brain responses can also be explained as a sequence of evoked responses, which only appear regular due to the rhythmicity of the stimulus, without necessarily involving underlying neural oscillations. To distinguish evoked responses from true oscillatory activity, we tested whether rhythmic stimulation produces oscillatory responses which continue after the end of the stimulus. Such sustained effects provide evidence for true involvement of neural oscillations. In Experiment 1, we found that rhythmic intelligible, but not unintelligible speech produces oscillatory responses in magnetoencephalography (MEG) which outlast the stimulus at parietal sensors. In Experiment 2, we found that transcranial alternating current stimulation (tACS) leads to rhythmic fluctuations in speech perception outcomes after the end of electrical stimulation. We further report that the phase relation between electroencephalography (EEG) responses and rhythmic intelligible speech can predict the tACS phase that leads to most accurate speech perception. Together, we provide fundamental results for several lines of research—including neural entrainment and tACS—and reveal endogenous neural oscillations as a key underlying principle for speech perception.

scholarly journals Sustained neural rhythms reveal endogenous oscillations supporting speech perception

2020 ◽  
Author(s):  
Sander van Bree ◽  
Ediz Sohoglu ◽  
Matthew H Davis ◽  
Benedikt Zoefel
Keyword(s):  
Electrical Stimulation ◽  
Speech Perception ◽  
Oscillatory Activity ◽  
Neural Oscillations ◽  
Evoked Responses ◽  
Sustained Effects ◽  
Brain Responses ◽  
Underlying Principle ◽  
Transcranial Alternating Current Stimulation ◽  
Intelligible Speech

AbstractRhythmic sensory or electrical stimulation will produce rhythmic brain responses. These rhythmic responses are often interpreted as endogenous neural oscillations aligned to the stimulus rhythm. However, stimulus-aligned brain responses can also be explained as a sequence of evoked responses, which only appear regular due to the rhythmicity of the stimulus, without necessarily involving underlying neural oscillations. To distinguish evoked responses from true oscillatory activity, we tested whether rhythmic stimulation produces oscillatory responses which continue after the end of the stimulus. Such sustained effects provide evidence for true involvement of neural oscillations. In Experiment 1, we found that rhythmic intelligible, but not unintelligible speech produces oscillatory responses in magnetoencephalography (MEG) which outlast the stimulus at parietal sensors. In Experiment 2, we found that transcranial alternating current stimulation (tACS) leads to rhythmic fluctuations in speech perception outcomes which continue after the end of electrical stimulation. We further report that the phase relation between electroencephalography (EEG) and rhythmic intelligible speech can predict the tACS phase that leads to most accurate speech perception. Together, our results lay the foundation for a new account of speech perception which includes endogenous neural oscillations as a key underlying principle.

scholarly journals Perception of Rhythmic Speech Is Modulated by Focal Bilateral Transcranial Alternating Current Stimulation

2020 ◽  
Vol 32 (2) ◽  
pp. 226-240 ◽  
Author(s):  
Benedikt Zoefel ◽  
Isobella Allard ◽  
Megha Anil ◽  
Matthew H. Davis
Keyword(s):  
Speech Perception ◽  
Speech Processing ◽  
Alternating Current ◽  
Stream Segregation ◽  
Causal Role ◽  
Oscillatory Activity ◽  
Transcranial Alternating Current Stimulation ◽  
Neural Entrainment ◽  
Actual Speech

Several recent studies have used transcranial alternating current stimulation (tACS) to demonstrate a causal role of neural oscillatory activity in speech processing. In particular, it has been shown that the ability to understand speech in a multi-speaker scenario or background noise depends on the timing of speech presentation relative to simultaneously applied tACS. However, it is possible that tACS did not change actual speech perception but rather auditory stream segregation. In this study, we tested whether the phase relation between tACS and the rhythm of degraded words, presented in silence, modulates word report accuracy. We found strong evidence for a tACS-induced modulation of speech perception, but only if the stimulation was applied bilaterally using ring electrodes (not for unilateral left hemisphere stimulation with square electrodes). These results were only obtained when data were analyzed using a statistical approach that was identified as optimal in a previous simulation study. The effect was driven by a phasic disruption of word report scores. Our results suggest a causal role of neural entrainment for speech perception and emphasize the importance of optimizing stimulation protocols and statistical approaches for brain stimulation research.

scholarly journals Neural entrainment determines the words we hear

2017 ◽  
Author(s):  
Anne Kösem ◽  
Hans Rutger Bosker ◽  
Atsuko Takashima ◽  
Antje Meyer ◽  
Ole Jensen ◽  
...  
Keyword(s):  
Speech Perception ◽  
Speech Processing ◽  
Speech Rate ◽  
Low Frequency ◽  
Acoustic Signals ◽  
Speech Analysis ◽  
Neural Dynamics ◽  
Neural Oscillations ◽  
Neural Entrainment ◽  
Perceived Duration

ABSTRACTLow-frequency neural entrainment to rhythmic input has been hypothesized as a canonical mechanism that shapes sensory perception in time. Neural entrainment is deemed particularly relevant for speech analysis, as it would contribute to the extraction of discrete linguistic elements from continuous acoustic signals. Yet, its causal influence in speech perception has been difficult to establish. Here, we provide evidence that oscillations build temporal predictions about the duration of speech tokens that directly influence perception. Using magnetoencephalography (MEG), we studied neural dynamics during listening to sentences that changed in speech rate. We observed neural entrainment to preceding speech rhythms persisting for several cycles after the change in rate. The sustained entrainment was associated with changes in the perceived duration of the last word’s vowel, resulting in the perception of words with radically different meanings. These findings support oscillatory models of speech processing, suggesting that neural oscillations actively shape speech perception.

scholarly journals Persistent neural entrainment in the human cortex is frequency selective

2019 ◽  
Author(s):  
Jacques Pesnot Lerousseau ◽  
Agnès Trébuchon ◽  
Benjamin Morillon ◽  
Daniele Schön
Keyword(s):  
Harmonic Oscillator ◽  
Low Frequency ◽  
Oscillatory Activity ◽  
Auditory Stimuli ◽  
Neural Oscillations ◽  
Human Cortex ◽  
Damped Harmonic Oscillator ◽  
High Gamma ◽  
Neural Entrainment ◽  
Frequency Selective

AbstractRhythmic stimulation, either sensory or electrical, aiming at entraining oscillatory activity to reveal or optimize brain functions, relies on a critically untested hypothesis: it should produce a persistent effect, outlasting the stimulus duration. We tested this assumption by studying cortical neural oscillations during and after presentation of rhythmic auditory stimuli. Using intracranial and surface recordings in humans, we reveal consistent neural response properties throughout the cortex, with persistent entrainment being selective to high-gamma oscillations. Critically, during passive perception, neural oscillations do not outlast low-frequency acoustic dynamics. We further show that our data are well-captured by a model of damped harmonic oscillator and can be classified into three classes of neural dynamics, with distinct damping properties and eigenfrequencies. This model thus provides a mechanistic and quantitative explanation of the frequency selectivity of persistent neural entrainment in the human cortex.Highlights- Neural oscillatory activity does not outlast low-frequency (2.5 Hz) acoustic dynamics during passive perception.- High-gamma activity is entrained by periodic auditory stimuli, with persistent activity up to 10 cycles after stimulus offset.- This frequency following response (FFR) is present throughout the cortex, up to inferior frontal and motor regions.- The frequency selective nature of neural entrainment is well-captured by a model of damped harmonic oscillator.

scholarly journals Multi-frequency tACS has lasting effects on neural synchrony and audiovisual responses

2019 ◽  
Author(s):  
Tobias Bockhorst ◽  
Joachim Ahlbeck ◽  
Florian Pieper ◽  
Gerhard Engler ◽  
Andreas K. Engel
Keyword(s):  
Electrical Stimulation ◽  
Cortical Network ◽  
Network Activity ◽  
Oscillatory Activity ◽  
Sensory Response ◽  
Audiovisual Stimulation ◽  
Gamma Range ◽  
Baseline Activity ◽  
Transcranial Alternating Current Stimulation ◽  
Audiovisual Processing

BACKGROUND: In cortical networks, synchronized oscillatory activity of neuronal populations enables communication, and its disturbance is related to a range of pathologies. Transcranial alternating current stimulation (tACS) has been explored as a flexible, noninvasive tool for the modulation and restoration of synchronized oscillatory signals. While numerous studies have addressed cognitive or behavioural effects of electrical stimulation, the neural changes underlying the effects of tACS and their persistence after stimulation offset have remained unclear. OBJECTIVE: Here, we screened for lasting aftereffects of prolonged tACS on intrinsic network activity and audiovisual processing in the anesthetized ferret brain. METHODS: Electrical stimulation was applied via subcutaneous wire electrodes. Current waveforms were synthesized from two frequencies in the alpha or gamma range, respectively. Flashes and clicks were used for audiovisual stimulation. Electrocorticographic recordings from an extended network including occipital, temporal and parietal cortical areas were obtained before and after tACS. RESULTS: Changes in local synchrony (continuous and spike-triggered power of LFP), synchrony across recording sites (imaginary coherence) and altered dynamics of sensory response-features (peak-to-peak amplitude, extremum latency) following electrical stimulation consistently point to a synchronizing effect of tACS that can outlast stimulation offset by at least 10 min. Gamma-band tACS proved particularly effective. In line with previous reports on cross-frequency interactions, we observed effects on coherence and power of baseline activity at frequencies other than the ones targeted by tACS. These cross-frequency interactions appeared to underlie the strengthening and stabilizing effect on audiovisual responses. CONCLUSION: We demonstrate aftereffects of tACS on synchrony and stimulus processing in an extended cortical network, measured intracranially in a setting that resembles tACS stimulation in humans. The data provide direct evidence for the efficacy of tACS as a tool for sustained modulation of cortical network dynamics.

scholarly journals Real-time suppression and amplification of frequency-specific neural activity using stimulation evoked oscillations

2020 ◽  
Author(s):  
David Escobar Sanabria ◽  
Luke A. Johnson ◽  
Ying Yu ◽  
Zachary Busby ◽  
Shane Nebeck ◽  
...  
Keyword(s):  
Electrical Stimulation ◽  
Real Time ◽  
Neural Control ◽  
Closed Loop ◽  
Low Frequency ◽  
Oscillatory Activity ◽  
Neural Oscillations ◽  
Optimization Approach ◽  
Electrode Arrays ◽  
Control Approach

AbstractBackgroundApproaches to predictably control neural oscillations are needed to understand their causal role in brain function in healthy or diseased states and to advance the development of neuromodulation therapies. In this study, we present a closed-loop neural control and optimization framework to actively suppress or amplify low-frequency neural oscillations observed in local field potentials in real-time by using electrical stimulation.Objective/HypothesisThe rationale behind this control approach and our working hypothesis is that neural oscillatory activity evoked by electrical pulses can suppress or amplify spontaneous oscillations via destructive or constructive interference when stimulation pulses are continuously delivered with appropriate amplitudes and at precise phases of these oscillations in a closed-loop scheme.MethodsWe tested our hypothesis in two nonhuman primates that exhibited a robust increase in low-frequency (8-30 Hz) oscillatory power in the subthalamic nucleus (STN) following administration of the neurotoxin 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP). To test our neural control approach, we targeted 8-17 Hz oscillations and used electrode arrays and electrical stimulation waveforms similar to those used in humans chronically implanted with brain stimulation systems. Stimulation parameters that maximize the suppression or amplification of neural oscillations were predicted using mathematical models of the stimulation evoked oscillations.ResultsOur neural control and optimization approach was capable of actively and robustly suppressing or amplifying oscillations in the targeted frequency band (8-17 Hz) in real-time in the studied subjects.ConclusionsThe results from this study support our hypothesis and suggest that the proposed neural control framework allows one to characterize in controlled experiments the functional role of frequency-specific neural oscillations by using electrodes and stimulation waveforms currently being employed in humans.

scholarly journals Toward integrative approaches to study the causal role of neural oscillations via transcranial electrical stimulation

2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Valeriia Beliaeva ◽  
Iurii Savvateev ◽  
Valerio Zerbi ◽  
Rafael Polania
Keyword(s):  
Electrical Stimulation ◽  
Causal Role ◽  
Neural Oscillations ◽  
Transcranial Electrical Stimulation ◽  
Integrative Research ◽  
Critical Issues ◽  
Neural Entrainment ◽  
Approaches To Study ◽  
Translational Approach

AbstractDiverse transcranial electrical stimulation (tES) techniques have recently been developed to elucidate the role of neural oscillations, but critically, it remains questionable whether neural entrainment genuinely occurs and is causally related to the resulting behavior. Here, we provide a perspective on an emerging integrative research program across systems, species, theoretical and experimental frameworks to elucidate the potential of tES to induce neural entrainment. We argue that such an integrative agenda is a requirement to establish tES as a tool to test the causal role of neural oscillations and highlight critical issues that should be considered when adopting a translational approach.

Neural Entrainment in Drum Rhythms with Silent Breaks: Evidence from Steady-state Evoked and Event-related Potentials

2016 ◽  
Vol 28 (12) ◽  
pp. 1865-1877 ◽  
Author(s):  
Jan Stupacher ◽  
Matthias Witte ◽  
Michael J. Hove ◽  
Guilherme Wood
Keyword(s):  
Steady State ◽  
Music Perception ◽  
Event Related Potentials ◽  
Stimulus Presentation ◽  
Oscillatory Activity ◽  
Neural Oscillations ◽  
Large Network ◽  
Neural Responses ◽  
Related Potentials ◽  
Neural Entrainment

The fusion of rhythm, beat perception, and movement is often summarized under the term “entrainment” and becomes obvious when we effortlessly tap our feet or snap our fingers to the pulse of music. Entrainment to music involves a large network of brain structures, and neural oscillations at beat-related frequencies can help elucidate how this network is connected. Here, we used EEG to investigate steady-state evoked potentials (SSEPs) and event-related potentials (ERPs) during listening and tapping to drum clips with different rhythmic structures that were interrupted by silent breaks of 2–6 sec. This design allowed us to address the question of whether neural entrainment processes persist after the physical presence of musical rhythms and to link neural oscillations and event-related neural responses. During stimulus presentation, SSEPs were elicited in both tasks (listening and tapping). During silent breaks, SSEPs were only present in the tapping task. Notably, the amplitude of the N1 ERP component was more negative after longer silent breaks, and both N1 and SSEP results indicate that neural entrainment was increased when listening to drum rhythms compared with an isochronous metronome. Taken together, this suggests that neural entrainment to music is not solely driven by the physical input but involves endogenous timing processes. Our findings break ground for a tighter linkage between steady-state and transient evoked neural responses in rhythm processing. Beyond music perception, they further support the crucial role of entrained oscillatory activity in shaping sensory, motor, and cognitive processes in general.

scholarly journals Perception of rhythmic speech is modulated by focal bilateral tACS

2019 ◽  
Author(s):  
Benedikt Zoefel ◽  
Isobella Allard ◽  
Megha Anil ◽  
Matthew H Davis
Keyword(s):  
Speech Perception ◽  
Speech Processing ◽  
Stream Segregation ◽  
Causal Role ◽  
Oscillatory Activity ◽  
Auditory Stream Segregation ◽  
Neural Entrainment ◽  
Actual Speech ◽  
Speech Presentation

AbstractSeveral recent studies have used transcranial alternating stimulation (tACS) to demonstrate a causal role of neural oscillatory activity in speech processing. In particular, it has been shown that the ability to understand speech in a multi-speaker scenario or background noise depends on the timing of speech presentation relative to simultaneously applied tACS. However, it is possible that tACS did not change actual speech perception but rather auditory stream segregation. In this study, we tested whether the phase relation between tACS and the rhythm of degraded words, presented in silence, modulates word report accuracy. We found strong evidence for a tACS-induced modulation of speech perception, but only if the stimulation was applied bilaterally using ring electrodes (not for unilateral left hemisphere stimulation with square electrodes). These results were only obtained when data was analyzed using a statistical approach that was identified as optimal in a previous simulation study. The effect was driven by a phasic disruption of word report scores. Our results suggest a causal role of neural entrainment for speech perception and emphasize the importance of optimizing stimulation protocols and statistical approaches for brain stimulation research.

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