Irregular speech rate dissociates auditory cortical entrainment, evoked responses, and frontal alpha

The entrainment of slow rhythmic auditory cortical activity to the temporal regularities in speech is considered to be a central mechanism underlying auditory perception. Previous work has shown that entrainment is reduced when the quality of the acoustic input is degraded, but has also linked rhythmic activity at similar time scales to the encoding of temporal expectations. To understand these bottom-up and top-down contributions to rhythmic entrainment, we manipulated the temporal predictive structure of speech by parametrically altering the distribution of pauses between syllables or words, thereby rendering the local speech rate irregular while preserving intelligibility and the envelope fluctuations of the acoustic signal. Recording EEG activity in human participants, we found that this manipulation did not alter neural processes reflecting the encoding of individual sound transients, such as evoked potentials. However, the manipulation significantly reduced the fidelity of auditory delta (but not theta) band entrainment to the speech envelope. It also reduced left frontal alpha power and this alpha reduction was predictive of the reduced delta entrainment across participants. Our results show that rhythmic auditory entrainment in delta and theta bands reflect functionally distinct processes. Furthermore, they reveal that delta entrainment is under top-down control and likely reflects prefrontal processes that are sensitive to acoustical regularities rather than the bottom-up encoding of acoustic features

Speech rhythms and multiplexed oscillatory sensory coding in the human brain

Cortical oscillations are likely candidates for segmentation and coding of continuous speech. Here, we monitored continuous speech processing with magnetoencephalography (MEG) to unravel the principles of speech segmentation and coding. We demonstrate that speech entrains the phase of low-frequency (delta, theta) and the amplitude of high-frequency (gamma) oscillations in the auditory cortex. Phase entrainment is stronger in the right and amplitude entrainment is stronger in the left auditory cortex. Furthermore, edges in the speech envelope phase reset auditory cortex oscillations thereby enhancing their entrainment to speech. This mechanism adapts to the changing physical features of the speech envelope and enables efficient, stimulus-specific speech sampling. Finally, we show that within the auditory cortex, coupling between delta, theta, and gamma oscillations increases following speech edges. Importantly, all couplings (i.e., brain-speech and also within the cortex) attenuate for backward-presented speech, suggesting top-down control. We conclude that segmentation and coding of speech relies on a nested hierarchy of entrained cortical oscillations

A new unifying account of the roles of neuronal entrainment

Rhythms are a fundamental and defining feature of neuronal activity in animals including humans. This rhythmic brain activity interacts in complex ways with rhythms in the internal and external environment through the phenomenon of ‘neuronal entrainment’, which is attracting increasing attention due to its suggested role in a multitude of sensory and cognitive processes. Some senses, such as touch and vision, sample the environment rhythmically, while others, like audition, are faced with mostly rhythmic inputs. Entrainment couples rhythmic brain activity to external and internal rhythmic events, serving fine-grained routing and modulation of external and internal signals across multiple spatial and temporal hierarchies. This interaction between a brain and its environment can be experimentally investigated and even modified by rhythmic sensory stimuli or invasive and non-invasive neuromodulation techniques. We provide a comprehensive overview of the topic and propose a theoretical framework of how neuronal entrainment dynamically structures information from incoming neuronal, bodily and environmental sources. We discuss the different types of neuronal entrainment, the conceptual advances in the field, and converging evidence for general principles

Investigating how neural entrainment relates to beat perception by disentangling the stimulus-driven response

Beat perception – the ability to perceive a steady pulse in music – is nearly ubiquitous in humans, but the neural mechanisms underlying this ability are unknown. A growing number of electroencephalography (EEG) studies suggest that beat perception is related to neural entrainment, a phenomenon in which cyclic changes in the excitability of populations of neurons synchronize with a rhythmic stimulus. However, the relationship between acoustically-driven and entrainment-driven neural activity is unclear. This thesis presents EEG research that extends our understanding neural entrainment is related to beat perception by characterizing, equating, and finally removing the stimulus-driven response in the neural signal isolating the entrainment-driven responses. Chapter 1 presents a general overview of how neural entrainment may relate to beat perception, the common methods of measuring neural entrainment, and current debates in the literature about how best to account for the stimulus-driven response in the neural signal and also what the neural power spectrum reflects. Chapter 2 presents research on how perceptual and acoustic factors in auditory stimuli influence neural spectral power in a series of experiments in which beat strength, tone duration, and onset/offset ramp duration were manipulated. The results suggest that both perceptual and acoustic factors influence neural spectral power, and that accounting for the stimulus-driven response in the neural spectrum is more complicated than previously assumed. Chapter 3 presents research on how power and phase of the neural signal relate to beat strength and beat location while controlling the stimulus-driven response. The results indicated a relationship between neural entrainment and beat strength, and also, between oscillatory phase and beat location. Chapter 4 presents research on the potential neural mechanisms of beat perception by examining neural activity during a silent immediately after rhythm perception for testing for ongoing, oscillatory activity. The results, although not statistically robust, suggest that entrained activity continues into silence, indicating a relationship between neural entrainment and beat perception. Chapter 5 presents a general discussion of Chapters 2-4 in the context of the existing literature, limitations, and broader interpretations of how these results relate to future directions in the field

Ultralow-frequency neural entrainment to pain

Nervous systems exploit regularities in the sensory environment to predict sensory input, 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., >0.5 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 ultralow-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 ultralow frequency did not entrain ultralow-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 ultralow-frequency entrainment might be tuned to the temporal scale of the statistical regularities characteristic of different sensory modalities

Phase entrainment and perceptual cycles in audition and vision

Des travaux récents indiquent qu'il existe des différences fondamentales entre les systèmes visuel et auditif: tandis que le premier semble échantillonner le flux d'information en provenance de l'environnement, en passant d'un "instantané" à un autre (créant ainsi des cycles perceptifs), la plupart des expériences destinées à examiner ce phénomène de discrétisation dans le système auditif ont mené à des résultats mitigés. Dans cette thèse, au travers de deux expériences de psychophysique, nous montrons que le sous-échantillonnage de l'information à l'entrée des systèmes perceptifs est en effet plus destructif pour l'audition que pour la vision. Cependant, nous révélons que des cycles perceptifs dans le système auditif pourraient exister à un niveau élevé du traitement de l'information. En outre, nos résultats suggèrent que du fait des fluctuations rapides du flot des sons en provenance de l'environnement, le système auditif tend à avoir son activité alignée sur la structure rythmique de ce flux. En synchronisant la phase des oscillations neuronales, elles-mêmes correspondant à différents états d'excitabilité, le système auditif pourrait optimiser activement le moment d'arrivée de ses "instantanés" et ainsi favoriser le traitement des informations pertinentes par rapport aux événements de moindre importance. Non seulement nos résultats montrent que cet entrainement de la phase des oscillations neuronales a des conséquences importantes sur la façon dont sont perçus deux flux auditifs présentés simultanément ; mais de plus, ils démontrent que l'entraînement de phase par un flux langagier inclut des mécanismes de haut niveau. Dans ce but, nous avons créé des stimuli parole/bruit dans lesquels les fluctuations de l'amplitude et du contenu spectral de la parole ont été enlevés, tout en conservant l'information phonétique et l'intelligibilité. Leur utilisation nous a permis de démontrer, au travers de plusieurs expériences, que le système auditif se synchronise à ces stimuli. Plus précisément, la perception, estimée par la détection d'un clic intégré dans les stimuli parole/bruit, et les oscillations neuronales, mesurées par Electroencéphalographie chez l'humain et à l'aide d'enregistrements intracrâniens dans le cortex auditif chez le singe, suivent la rythmique "de haut niveau" liée à la parole. En résumé, les résultats présentés ici suggèrent que les oscillations neuronales sont un mécanisme important pour la discrétisation des informations en provenance de l'environnement en vue de leur traitement par le cerveau, non seulement dans la vision, mais aussi dans l'audition. Pourtant, il semble exister des différences fondamentales entre les deux systèmes: contrairement au système visuel, il est essentiel pour le système auditif de se synchroniser (par entraînement de phase) à son environnement, avec un échantillonnage du flux des informations vraisemblablement réalisé à un niveau hiérarchique élevé.Recent research indicates fundamental differences between the auditory and visual systems: Whereas the visual system seems to sample its environment, cycling between "snapshots" at discrete moments in time (creating perceptual cycles), most attempts at discovering discrete perception in the auditory system failed. Here, we show in two psychophysical experiments that subsampling the very input to the visual and auditory systems is indeed more disruptive for audition; however, the existence of perceptual cycles in the auditory system is possible if they operate on a relatively high level of auditory processing. Moreover, we suggest that the auditory system, due to the rapidly fluctuating nature of its input, might rely to a particularly strong degree on phase entrainment, the alignment between neural activity and the rhythmic structure of its input: By using the low and high excitability phases of neural oscillations, the auditory system might actively control the timing of its "snapshots" and thereby amplify relevant information whereas irrelevant events are suppressed. Not only do our results suggest that the oscillatory phase has important consequences on how simultaneous auditory inputs are perceived; additionally, we can show that phase entrainment to speech sound does entail an active high-level mechanism. We do so by using specifically constructed speech/noise sounds in which fluctuations in low-level features (amplitude and spectral content) of speech have been removed, but intelligibility and high-level features (including, but not restricted to phonetic information) have been conserved. We demonstrate, in several experiments, that the auditory system can entrain to these stimuli, as both perception (the detection of a click embedded in the speech/noise stimuli) and neural oscillations (measured with electroencephalography, EEG, and in intracranial recordings in primary auditory cortex of the monkey) follow the conserved "high-level" rhythm of speech. Taken together, the results presented here suggest that, not only in vision, but also in audition, neural oscillations are an important tool for the discretization and processing of the brain's input. However, there seem to be fundamental differences between the two systems: In contrast to the visual system, it is critical for the auditory system to adapt (via phase entrainment) to its environment, and input subsampling is done most likely on a hierarchically high level of stimulus processing

Ultralow-frequency neural entrainment to pain

Nervous systems exploit regularities in the sensory environment to predict sensory input, 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., >0.5 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 ultralow-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 ultralow frequency did not entrain ultralow-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 ultralow-frequency entrainment might be tuned to the temporal scale of the statistical regularities characteristic of different sensory modalities

No changes in parieto-occipital alpha during neural phase locking to visual quasi-periodic theta-, alpha-, and beta-band stimulation

Recent studies have probed the role of the parieto‐occipital alpha rhythm (8 – 12 Hz) in human visual perception through attempts to drive its neural generators. To that end, paradigms have used high‐intensity strictly‐periodic visual stimulation that created strong predictions about future stimulus occurrences and repeatedly demonstrated perceptual consequences in line with an entrainment of parieto‐occipital alpha. Our study, in turn, examined the case of alpha entrainment by non‐predictive low‐intensity quasi‐periodic visual stimulation within theta‐ (4 – 7 Hz), alpha‐ (8 – 13 Hz) and beta (14 – 20 Hz) frequency bands, i.e. a class of stimuli that resemble the temporal characteristics of naturally occurring visual input more closely. We have previously reported substantial neural phase‐locking in EEG recording during all three stimulation conditions. Here, we studied to what extent this phase‐locking reflected an entrainment of intrinsic alpha rhythms in the same dataset. Specifically, we tested whether quasi‐periodic visual stimulation affected several properties of parieto‐occipital alpha generators. Speaking against an entrainment of intrinsic alpha rhythms by non‐predictive low‐intensity quasi‐periodic visual stimulation, we found none of these properties to show differences between stimulation frequency bands. In particular, alpha band generators did not show increased sensitivity to alpha band stimulation and Bayesian inference corroborated evidence against an influence of stimulation frequency. Our results set boundary conditions for when and how to expect effects of entrainment of alpha generators and suggest that the parieto‐occipital alpha rhythm may be more inert to external influences than previously thought

Speech-brain synchronization: a possible cause for developmental dyslexia

152 p.Dyslexia is a neurological learning disability characterized by the difficulty in an individual¿s ability to read despite adequate intelligence and normal opportunities. The majority of dyslexic readers present phonological difficulties. The phonological difficulty most often associated with dyslexia is a deficit in phonological awareness, that is, the ability to hear and manipulate the sound structure of language. Some appealing theories of dyslexia attribute a causal role to auditory atypical oscillatory neural activity, suggesting it generates some of the phonological problems in dyslexia. These theories propose that auditory cortical oscillations of dyslexic individuals entrain less accurately to the spectral properties of auditory stimuli at distinct frequency bands (delta, theta and gamma) that are important for speech processing. Nevertheless, there are diverging hypotheses concerning the specific bands that would be disrupted in dyslexia, and which are the consequences of such difficulties on speech processing. The goal of the present PhD thesis was to portray the neural oscillatory basis underlying phonological difficulties in developmental dyslexia. We evaluated whether phonological deficits in developmental dyslexia are associated with impaired auditory entrainment to a specific frequency band. In that aim, we measured auditory neural synchronization to linguistic and non-linguistic auditory signals at different frequencies corresponding to key phonological units of speech (prosodic, syllabic and phonemic information). We found that dyslexic readers presented atypical neural entrainment to delta, theta and gamma frequency bands. Importantly, we showed that atypical entrainment to theta and gamma modulations in dyslexia could compromise perceptual computations during speech processing, while reduced delta entrainment in dyslexia could affect perceptual and attentional operations during speech processing. In addition, we characterized the links between the anatomy of the auditory cortex and its oscillatory responses, taking into account previous studies which have observed structural alterations in dyslexia. We observed that the cortical pruning in auditory regions was linked to a stronger sensitivity to gamma oscillation in skilled readers, but to stronger theta band sensitivity in dyslexic readers. Thus, we concluded that the left auditory regions might be specialized for processing phonological information at different time scales (phoneme vs. syllable) in skilled and dyslexic readers. Lastly, by assessing both children and adults on similar tasks, we provided the first evaluation of developmental modulations of typical and atypical auditory sampling (and their structural underpinnings). We found that atypical neural entrainment to delta, theta and gamma are present in dyslexia throughout the lifespan and is not modulated by reading experience