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

2019 ◽  
Author(s):  
Jacques Pesnot Lerousseau ◽  
Agnès Trébuchon ◽  
Benjamin Morillon ◽  
Daniele Schön

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.

2015 ◽  
Vol 112 (45) ◽  
pp. E6233-E6242 ◽  
Author(s):  
Keith B. Doelling ◽  
David Poeppel

Recent studies establish that cortical oscillations track naturalistic speech in a remarkably faithful way. Here, we test whether such neural activity, particularly low-frequency (<8 Hz; delta–theta) oscillations, similarly entrain to music and whether experience modifies such a cortical phenomenon. Music of varying tempi was used to test entrainment at different rates. In three magnetoencephalography experiments, we recorded from nonmusicians, as well as musicians with varying years of experience. Recordings from nonmusicians demonstrate cortical entrainment that tracks musical stimuli over a typical range of tempi, but not at tempi below 1 note per second. Importantly, the observed entrainment correlates with performance on a concurrent pitch-related behavioral task. In contrast, the data from musicians show that entrainment is enhanced by years of musical training, at all presented tempi. This suggests a bidirectional relationship between behavior and cortical entrainment, a phenomenon that has not previously been reported. Additional analyses focus on responses in the beta range (∼15–30 Hz)—often linked to delta activity in the context of temporal predictions. Our findings provide evidence that the role of beta in temporal predictions scales to the complex hierarchical rhythms in natural music and enhances processing of musical content. This study builds on important findings on brainstem plasticity and represents a compelling demonstration that cortical neural entrainment is tightly coupled to both musical training and task performance, further supporting a role for cortical oscillatory activity in music perception and cognition.


2019 ◽  
Author(s):  
Jonathan Daume ◽  
Peng Wang ◽  
Alexander Maye ◽  
Dan Zhang ◽  
Andreas K. Engel

AbstractThe phase of neural oscillatory activity aligns to the predicted onset of upcoming stimulation. Whether such phase alignments represent phase resets of underlying neural oscillations or just rhythmically evoked activity, and whether they can be observed in a rhythm-free visual context, however, remains unclear. Here, we recorded the magnetoencephalogram while participants were engaged in a temporal prediction task judging the visual or tactile reappearance of a uniformly moving stimulus. The prediction conditions were contrasted with a control condition to dissociate phase adjustments of neural oscillations from stimulus-driven activity. We observed stronger delta band inter-trial phase consistency (ITPC) in a network of sensory, parietal and frontal brain areas, but no power increase reflecting stimulus-driven or prediction-related processes. Delta ITPC further correlated with prediction performance in the cerebellum and visual cortex. Our results provide evidence that phase alignments of low-frequency neural oscillations underlie temporal predictions in a non-rhythmic visual and crossmodal context.


2017 ◽  
Author(s):  
Anne Kösem ◽  
Hans Rutger Bosker ◽  
Atsuko Takashima ◽  
Antje Meyer ◽  
Ole Jensen ◽  
...  

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.


PLoS Biology ◽  
2021 ◽  
Vol 19 (2) ◽  
pp. e3001142
Author(s):  
Sander van Bree ◽  
Ediz Sohoglu ◽  
Matthew H. Davis ◽  
Benedikt Zoefel

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.


2020 ◽  
Vol 123 (3) ◽  
pp. 1063-1071
Author(s):  
Indiana Wollman ◽  
Pablo Arias ◽  
Jean-Julien Aucouturier ◽  
Benjamin Morillon

During auditory perception, neural oscillations are known to entrain to acoustic dynamics but their role in the processing of auditory information remains unclear. As a complex temporal structure that can be parameterized acoustically, music is particularly suited to address this issue. In a combined behavioral and EEG experiment in human participants, we investigated the relative contribution of temporal (acoustic dynamics) and nontemporal (melodic spectral complexity) dimensions of stimulation on neural entrainment, a stimulus-brain coupling phenomenon operationally defined here as the temporal coherence between acoustical and neural dynamics. We first highlight that low-frequency neural oscillations robustly entrain to complex acoustic temporal modulations, which underscores the fine-grained nature of this coupling mechanism. We also reveal that enhancing melodic spectral complexity, in terms of pitch, harmony, and pitch variation, increases neural entrainment. Importantly, this manipulation enhances activity in the theta (5 Hz) range, a frequency-selective effect independent of the note rate of the melodies, which may reflect internal temporal constraints of the neural processes involved. Moreover, while both emotional arousal ratings and neural entrainment were positively modulated by spectral complexity, no direct relationship between arousal and neural entrainment was observed. Overall, these results indicate that neural entrainment to music is sensitive to the spectral content of auditory information and indexes an auditory level of processing that should be distinguished from higher-order emotional processing stages. NEW & NOTEWORTHY Low-frequency (<10 Hz) cortical neural oscillations are known to entrain to acoustic dynamics, the so-called neural entrainment phenomenon, but their functional implication in the processing of auditory information remains unclear. In a behavioral and EEG experiment capitalizing on parameterized musical textures, we disentangle the contribution of stimulus dynamics, melodic spectral complexity, and emotional judgments on neural entrainment and highlight their respective spatial and spectral neural signature.


2016 ◽  
Vol 78 (6-8) ◽  
Author(s):  
Nor Azila Noh ◽  
Azlina Mokhtar ◽  
Nazefah Abdul Hamid ◽  
Mohd Dzulkhairi Mohd Rani ◽  
Nor Aripin Shamaan

Disturbance in brain oscillations is observed in many neuropsychiatric disorders. Any tool that has the potential to restore abnormal brain oscillations is therefore beneficial to patients with neuropsychiatric illnesses. Repetitive transcranial magnetic stimulation (rTMS) is one such tool. It is a non-invasive brain stimulation technique, which is able to alter brain oscillations depending on its parameters of stimulation and is used in clinical setting because of its potential therapeutic effects on the brain. However, the optimum stimulation parameters to induce the therapeutic effect of rTMS remains elusive. Therefore, it is important to investigate the differential effects between high versus low frequency of magnetic stimulation on the mechanism of brain oscillations in human subjects. Here we show, using combined rTMS and surface electroencephalography (EEG) that low and high frequencies of magnetic stimulation would induce dichotomy effects in EEG brain oscillatory activity. In particular, high-frequency rTMS 10Hz induces a synchronised oscillations for theta brain rhythm. In contrast, low-frequency rTMS 1Hz desynchronises neural oscillations on the same brain rhythm. Taken together, our results show that the desynchronisation effect of low-frequency rTMS 1Hz may potentially reverse the interference of altered neural oscillations. More extensive basic and clinical research using combined rTMS and EEG are needed to determine the optimum parameters of rTMS stimulation to restore adequate neural oscillations.


2016 ◽  
Vol 28 (12) ◽  
pp. 1865-1877 ◽  
Author(s):  
Jan Stupacher ◽  
Matthias Witte ◽  
Michael J. Hove ◽  
Guilherme Wood

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.


2019 ◽  
Author(s):  
Y Guo ◽  
RJ Bufacchi ◽  
G Novembre ◽  
M Kilintari ◽  
M Moayedi ◽  
...  

AbstractNervous systems exploit regularities in the sensory environment to predict sensory input and adjust behavior, and thereby maximize fitness. Entrainment of neural oscillations allows retaining temporal regularities of sensory information, a prerequisite for prediction. Entrainment has been extensively described at the frequencies of periodic inputs most commonly present in visual and auditory landscapes (e.g. >1 Hz). An open question is whether neural entrainment also occurs for regularities at much longer timescales. Here we exploited the fact that the temporal dynamics of thermal stimuli in natural environment can unfold very slowly. We show that ultra-low frequency neural oscillations preserved a long-lasting trace of sensory information through neural entrainment to periodic thermo-nociceptive input as low as 0.1 Hz. Importantly, revealing the functional significance of this phenomenon, both power and phase of the entrainment predicted individual pain sensitivity. In contrast, periodic auditory input at the same ultra-low frequency did not entrain ultra-low frequency oscillations. These results demonstrate that a functionally-significant neural entrainment can occur at temporal scales far longer than those commonly explored. The non-supramodal nature of our results suggests that ultra-low frequency entrainment might be tuned to the temporal scale of the statistical regularities characteristic of different sensory modalities.


Author(s):  
David Escobar Sanabria ◽  
Luke A. Johnson ◽  
Ying Yu ◽  
Zachary Busby ◽  
Shane Nebeck ◽  
...  

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.


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