Repetition suppression comprises both attention-independent and attention-dependent processes

International audienceRepetition suppression, a robust phenomenon of reduction in neural responses to stimulus repetition, is suggested to consist of a combination of bottom-up adaptation and top-down prediction effects. However, there is little consensus on how repetition suppression is related to attention in functional magnetic resonance imaging (fMRI) studies. It is probably because fMRI integrates neural activity related to adaptation and prediction effects, which are respectively attention-independent and attention-dependent. Here we orthogonally manipulated stimulus repetition and attention in a target detection task while participants' electroencephalography (EEG) was recorded. In Experiment 1, we found a significant repetition effect on N1 amplitude regardless of attention, whereas the repetition effect on P2 amplitude was attention-dependent. In Experiment 2 where the attentional manipulation was more stringent than that in Experiment 1, we replicated a significant repetition effect on N1 amplitude regardless of attention, whereas the repetition effect on P2 amplitude was eliminated. The results show that repetition suppression comprises both attention-independent and attention-dependent components

Neural Responses to Novel and Existing Words in Children with Autism Spectrum and Developmental Language Disorder

\ua9 2021, the Authors.The formation of new phonological representations is key in establishing items in the mental lexicon. Phonological forms become stable with repetition, time and sleep. Atypicality in the establishment of new word forms is characteristic of children with developmental language disorder (DLD) and autism spectrum disorder (ASD), yet neural changes in response to novel word forms over time have not yet been directly compared in these groups. This study measured habituation of event-related-potentials (ERPs) to novel and known words within and between two sessions spaced 24 hours apart in typically developing (TD) children, and their peers with DLD or ASD. We hypothesised that modulation of the auditory N400 amplitude would mark real-time changes in lexical processing with habituation evident within and across sessions in the TD group, while the DLD group would show attenuated habituation within sessions, and the ASD group attenuated habituation between sessions. Twenty-one typically developing children, 19 children with ASD, and 16 children with DLD listened passively to known and novel words on two consecutive days, while ERPs were recorded using dry electrodes. Counter to our hypotheses, no habituation effect emerged within sessions. However, responses did habituate between sessions, with this effect being reduced in the DLD group, indicating less pre-activation of lexical representations in response to words encountered the previous day. No differences in change over time were observed between the TD and ASD groups. These data are in keeping with theories stressing the importance of sleep-related consolidation in word learning

Prior Precision Modulates the Minimization of Auditory Prediction Error

The predictive coding model of perception proposes that successful representation of the perceptual world depends upon canceling out the discrepancy between prediction and sensory input (i.e., prediction error). Recent studies further suggest a distinction to be made between prediction error triggered by non-predicted stimuli of different prior precision (i.e., inverse variance). However, it is not fully understood how prediction error with different precision levels is minimized in the predictive process. Here, we conducted a magnetoencephalography (MEG) experiment which orthogonally manipulated prime-probe relation (for contextual precision) and stimulus repetition (for perceptual learning which decreases prediction error). We presented participants with cycles of tone quartets which consisted of three prime tones and one probe tone of randomly selected frequencies. Within each cycle, the three prime tones remained identical while the probe tones changed once at some point (e.g., from repetition of 123X to repetition of 123Y). Therefore, the repetition of probe tones can reveal the development of perceptual inferences in low and high precision contexts depending on their position within the cycle. We found that the two conditions resemble each other in terms of N1m modulation (as both were associated with N1m suppression) but differ in terms of N2m modulation. While repeated probe tones in low precision context did not exhibit any modulatory effect, repeated probe tones in high precision context elicited a suppression and rebound of the N2m source power. The differentiation suggested that the minimization of prediction error in low and high precision contexts likely involves distinct mechanisms

Neural Responses to Novel and Existing Words in Children with Autism Spectrum and Developmental Language Disorder

The formation of new phonological representations is key in establishing items in the mental lexicon. Phonological forms become stable with repetition, time and sleep. Atypicality in the establishment of new word forms is characteristic of children with developmental language disorder (DLD) and autism spectrum disorder (ASD), yet neural changes in response to novel word forms over time have not yet been directly compared in these groups. This study measured habituation of event-related-potentials (ERPs) to novel and known words within and between two sessions spaced 24 hours apart in typically developing (TD) children, and their peers with DLD or ASD. We hypothesised that modulation of the auditory N400 amplitude would mark real-time changes in lexical processing with habituation evident within and across sessions in the TD group, while the DLD group would show attenuated habituation within sessions, and the ASD group attenuated habituation between sessions. Twenty-one typically developing children, 19 children with ASD, and 16 children with DLD listened passively to known and novel words on two consecutive days, while ERPs were recorded using dry electrodes. Counter to our hypotheses, no habituation effect emerged within sessions. However, responses did habituate between sessions, with this effect being reduced in the DLD group, indicating less pre-activation of lexical representations in response to words encountered the previous day. No differences in change over time were observed between the TD and ASD groups. These data are in keeping with theories stressing the importance of sleep-related consolidation in word learning

The Role of Action-Effect Contingency on Sensory Attenuation in the Absence of Movement

Stimuli that have been generated by a person's own willed motor actions generally elicit a suppressed electrophysiological, as well as phenomenological, response than identical stimuli that have been externally generated. This well-studied phenomenon, known as sensory attenuation, has mostly been studied by comparing ERPs evoked by self-initiated and externally generated sounds. However, most studies have assumed a uniform action–effect contingency, in which a motor action leads to a resulting sensation 100% of the time. In this study, we investigated the effect of manipulating the probability of action–effect contingencies on the sensory attenuation effect. In Experiment 1, participants watched a moving, marked tickertape while EEG was recorded. In the full-contingency (FC) condition, participants chose whether to press a button by a certain mark on the tickertape. If a button press had not occurred by the mark, a sound would be played a second later 100% of the time. If the button was pressed before the mark, the sound was not played. In the no-contingency (NC) condition, participants observed the same tickertape; in contrast, however, if participants did not press the button by the mark, a sound would occur only 50% of the time (NC-inaction). Furthermore, in the NC condition, if a participant pressed the button before the mark, a sound would also play 50% of the time (NC-action). In Experiment 2, the design was identical, except that a willed action (as opposed to a willed inaction) triggered the sound in the FC condition. The results were consistent across the two experiments: Although there were no differences in N1 amplitude between conditions, the amplitude of the Tb and P2 components were smaller in the FC condition compared with the NC-inaction condition, and the amplitude of the P2 component was also smaller in the FC condition compared with the NC-action condition. The results suggest that the effect of contingency on electrophysiological indices of sensory attenuation may be indexed primarily by the Tb and P2 components, rather than the N1 component which is most commonly studied

An electrophysiological investigation into the role of agency and contingency on sensory attenuation

Stimuli generated by a person’s own willed actions generally elicit a suppressed neurophysiological response than physically identical stimuli that have been externally generated. This phenomenon, known as sensory attenuation, has primarily been studied by comparing the N1, Tb and P2 components of the event-related potentials (ERPs) evoked by self-initiated vs. externally generated sounds. Sensory attenuation has been implicated in some psychotic disorders such as schizophrenia, where symptoms such as auditory hallucinations and delusions of control have been conceptualised as reflecting a difficulty in distinguishing between internally and externally generated stimuli. This thesis employed a novel paradigm across five experiments to investigate the role of agency and contingency in sensory attenuation. The role of agency was investigated in in Chapter 2. In Experiment 1, participants watched a moving, marked tickertape while EEG was recorded. In the active condition, participants chose whether to press a button by a certain mark on the tickertape. If a button-press had not occurred by the mark, then a tone would be played one second later. If the button was pressed prior to the mark, the tone was not played. In the passive condition, participants passively watched the animation, and were informed about whether a tone would be played on each trial. The design for Experiment 2 was identical, except that the contingencies were reversed (i.e., pressing the button prior to the mark led to a tone). The results were consistent across the two experiments: while there were no differences in N1 amplitude between the active and passive conditions, the amplitude of the Tb component was suppressed in the active condition. The amplitude of the P2 component was enhanced in the active condition in both Experiments 1 and 2. These results suggest that agency and motor actions per se have differential effects on sensory attenuation to sounds and are indexed with different ERP components. In Chapter 3, we investigated the role of contingency in sensory attenuation while using a similar ticker-tape design in Chapter 2. In the Full Contingency (FC) condition, participants again chose whether to press a button by a certain mark on the tickertape. If a button-press had not occurred by the mark, a sound would be played (one second later) 100% of the time (Experiment 3). If the button was pressed prior to the mark, the sound was not played. In the Half Contingency (HC) condition, participants observed the same tickertape; however, if participants did not press the button by the mark, a sound would occur 50% of the time (HC-Inaction) while if the participant did press the button, a sound would also play 50% of the time (HC-Action). In Experiment 4, the design was identical, except that a button-press triggered the sound in the FC condition. The results were consistent across both Experiments in Chapter 3: while there were no differences in N1 amplitude across the FC and HC conditions, the amplitude of the Tb component was smaller in the FC condition when compared to the HC-Inaction condition. The amplitude of the P2 component was also smaller in the FC condition compared to both the HC-Action and HC-Inaction conditions. The results suggest that the effect of contingency on neurophysiological indices of sensory attenuation may be indexed by the Tb and P2 components, as opposed to the more heavily studied N1 component. Chapter 4 also investigated contingency but instead used a more ‘traditional’ self-stimulation paradigm, in which sounds immediately followed the button-press. In Chapter 4, participants observed a fixation cross while pressing a button to generate a sound. The probability of the sound occurring after the button-press was either 100% (active 100) or 50% (active 50). In the two passive conditions (passive 100 and passive 50), sounds generated in the corresponding active conditions were recorded and played back to participants while they passively listened. In contrast with the results of Chapter 3, the results of Chapter 4 showed both the classical N1 suppression effect, and also an effect of contingency of the N1, where sounds with a 50% probability generated higher N1 amplitudes compared to sounds with 100% probability. In contrast, Tb amplitude was modulated by contingency but did not show any differences between the active and passive conditions. The results of this study suggest that both sense of agency and sensory contingency can influence sensory attenuation, and thus should be considered in future studies investigating this theoretically and clinically important phenomenon

Integrative function in rat visual system

A vital function of the brain is to acquire information about the events in the environment and to respond appropriately. The brain needs to integrate the incoming information from multiple senses to improve the quality of the sensory signal. It also needs to be able to distribute the processing resources to optimise the integration across modalities based on the reliability and salience of the incoming signals. This thesis aimed to investigate two aspects of the way in which the brain integrates information from the external environment: multisensory integration and selective attention. The hooded rat was used as the experimental animal model. In Chapter 2 of this thesis, I investigate the multisensory properties of neurons in superior colliculus (SC), a midbrain structure involved in attentive and orienting behaviours. I first establish that in rat SC, spiking activity is elevated by whisker or visual stimuli, but rarely both, when those stimuli are presented in isolation. I then show that visually responsive sites are mainly found in superficial layers whereas whisker responsive sites were in intermediate layers. Finally I show that there are robust suppressive interactions between these two modalities. In Chapter 3, I develop a rodent behavioural paradigm that can easily be paired with electrophysiological measurements. The design is adaptable to a variety of detection and discrimination tasks. Head position is restricted in the central nose-poke without head-fixation and the eyes can be constantly monitored via video camera. In Chapter 4, I ask whether selective spatial visual attention can be demonstrated in rats utilising the paradigms developed in Chapter 3. Selective attention is the process by which brain focuses on significant external events. Does being able to predict the likely side of the stimulus modulate the speed and accuracy of stimulus detection? To address this question, I varied the probability with which the signal was presented on left or right screen. My results suggest that rats have the capacity for spatial attention engaged by top-down mechanisms that have access to the predictability of stimulus location. In summary, my thesis presents a paradigm to study visual behaviour, multisensory integration and selective spatial attention in rats. Over the last decade, rats have gained popularity as a viable animal model in sensory systems neuroscience because of the access to the array of genetic tools and in vivo electrophysiology and imaging techniques. As such the paradigms developed here provide a useful preparation to complement the existing well-established primate models

Compréhension intégrée de quatre syndromes génétiques impliqués dans la déficience intellectuelle via des biomarqueurs électrophysiologiques, les manifestations comportementales, le fonctionnement adaptatif et les interventions disponibles sur le plan clinique.

La trisomie 21 (T21), le Syndrome X Fragile (SXF), la Sclérose tubéreuse de Bourneville (STB) et les mutations SYNGAP1 sont causés par des dysfonctionnements des voies moléculaires qui entraînent notamment un déséquilibre dans l’excitation et l’inhibition de l’activité neuronale qui aurait des impacts sur le développement et le fonctionnement du cerveau. Toutefois, il est difficile de faire le pont entre les déséquilibres moléculaires observés dans les modèles animaux et les particularités structurelles, fonctionnelles et cognitives observées dans ces syndromes chez l’humain. À notre connaissance, peu d’études ont comparé différents syndromes génétiques sur les processus sensoriels, l’apprentissage de base ou encore leurs caractéristiques comportementales en utilisant des paradigmes similaires et translationnels, permettant de mieux comprendre leurs particularités. Le premier volet de cette thèse vise à identifier si l’activité électroencéphalographique serait un biomarqueur adéquat représentant les altérations neurobiologiques tant des processus sensoriels que d’apprentissage chez les humains présentant ces syndromes. L’étude #1 avait comme objectif de décrire le traitement sensoriel auditif, comme il s’agit d’un processus élémentaire, et ce, chez les mutations SYNGAP1 qui représentent une condition génétique encore peu étudiée chez l’humain. Les résultats ont d’ailleurs permis d’identifier une diminution de la synchronisation de phase et une augmentation de la puissance dans la bande gamma qui distinguent cette condition génétique tant des participants sans DI que de la T21. Toujours dans l’esprit d’identifier des biomarqueurs électroencéphalographiques, mais cette fois au niveau d’un processus cognitif de base, l’étude #2 avait pour objectif de comparer tous ces syndromes dans un paradigme de suppression neuronale (SN) afin de vérifier la présence de SN et de comparer l’apprentissage de base chez ces populations. Les résultats ont identifiés que la T21 et le SXF présentaient tous les deux un patron de SN et que le SXF présentait relativement une plus forte habituation indiquant des particularités spécifiques selon les syndromes. Le deuxième volet, davantage clinique, permet de comparer les profils comportementaux associés au fonctionnement adaptatif entre les syndromes et à décrire les pistes d’intervention existantes. L’étude #3 a notamment mis en évidence que le QI et les symptômes de TDAH sont associés au fonctionnement adaptatif auprès de ces différents syndromes dont le SXF et la STB. Cet article a aussi permis de décrire les profils comportementaux de ces mêmes conditions en révélant davantage de difficultés rapportées chez les individus présentant un SXF, alors que la T21 présentait moins de particularités cliniques au niveau comportemental. Enfin, l’article #4 a mis en lumière diverses interventions utilisées auprès de la population présentant une DI notamment des stratégies cognitivo-comportementales et compensatoires. Cette thèse permet donc de dresser un portrait spécifique de ces syndromes génétiques concernant leur signature électrophysiologique lors du traitement sensoriel et de l’apprentissage ainsi que sur le plan des comorbidités comportementales et de leur relation avec le fonctionnement adaptatif, pour ensuite aborder les interventions actuelles en DI. Les diverses particularités identifiées à plusieurs niveaux ont permis de générer des suggestions pouvant guider certaines interventions futures.Down syndrome (DS), Fragile X syndrome (FXS), Tuberous sclerosis complex (TSC) and SYNGAP1 mutations are caused by dysfunctions of the molecular pathways which lead among others to an imbalance in excitation and inhibition of the neuronal activity that would impact the brain development and its functioning. However, it is difficult to directly bridge the gap between the molecular imbalances observed in animal models with the structural, functional and cognitive characteristics observed in human with these syndromes. To our knowledge, few studies have compared those different genetic syndromes on sensory processing, basic learning or on their behavioural issues using similar and translational paradigms then allowing a better understanding of their specificities. The first part of this thesis aims to identify whether electroencephalographic activity would be an adequate biomarker representing neurobiological alterations both in sensory processing and learning in humans with these syndromes. The goal of study #1 was to describe auditory sensory processing, as a very first basic process, in SYNGAP1 mutations being a genetic condition still little studied in humans. Results showed a decrease in phase synchronization and an increase in the power of gamma band which distinguish this genetic condition both from participants without ID and from DS. Still in order to identify electroencephalographic biomarkers, but this time at a basic cognitive level, study #2 aimed to compare all these syndromes in a repetition suppression (RS) paradigm in order to observe the presence of RS and compare basic learning in these populations. The results identified a RS pattern in both DS and FXS. FXS also exhibited relatively higher habituation then indicating specific features according to the syndrome. The second part, addressing clinical aspects, permits to compare the behavioural profiles associated with adaptive functioning between syndromes and to describe existing interventions on ID population. Study #3 notably highlighted that IQ and ADHD symptoms are associated with adaptive functioning especially in FXS and TSC. This article also made it possible to describe the behavioural profiles of these syndromes, revealing more difficulties reported in individuals with FXS, while DS presented fewer behavioural issues. Finally, article #4 highlighted various interventions used with ID population, notably cognitive-behavioural and compensatory strategies. This thesis therefore makes it possible to gain a better understanding of these genetic syndromes concerning their electrophysiological signature during sensory processing and learning as well as in terms of behavioural comorbidities and their relationship with adaptive functioning, to then address current ID interventions. These different syndromic particularities identified at several levels made it possible to generate suggestions that could guide future interventions in this field

A Comparison of Perceptual and Semantic Priming

Masked Priming is an established paradigm to investigate consciousness. The impact of prime visibility on specific priming effects determines whether associated processes can occur independently of consciousness or might rely on consciousness. A meta-analytic review of 84 studies was conducted to assess the impact of prime visibility on effect sizes in interaction with various moderators (Chapter 2). A psychological model concerning the emergence of priming effects was proposed. Two main confoundings between moderators were identified. Specific task levels were predominantly applied with specific masking methods. Furthermore, temporal parameters were chosen differently between effect types. Subsequent experiments (Chapter 3) revealed that priming effects increase with increasing prime visibility when pattern masks are applied. Priming effects were independent of prime visibility with metacontrast masks. Pattern masks are thought to reduce prime visibility on an early level whereas metacontrast masks disturb recurrent processing. Lamme and Roelfsema (2000) previously proposed that recurrent processing characterizes consciousness. Perceptual and semantic priming effects were equally affected by variations in prime visibility. However, perceptual priming effects were generally larger than semantic priming effects. Further experiments were conducted to determine the courses of perceptual and semantic priming effects with increasing prime-mask SOA and mask-target SOA (Chapter 4). Priming effects generally increase with increasing prime-mask SOA and decline at long mask-target SOA. This decline seems to be based on a simple decay and active mechanisms of inhibition (e.g. Klapp, 2005). However, courses of perceptual and semantic priming effects with increasing mask-target SOA differed. This seems to be due to an additional mechanism of object updating that acts only with relevant masks (Lleras & Enns, 2004). In the current design, masks only activated the incongruent category (i.e. relevant masks) with perceptual congruency. An electrophysiological study was conducted to compare perceptual and semantic priming with identical stimulation (Chapter 5). The applied design allowed the estimation of behavioral priming effects without response association as well as effects on event-related potentials without response execution. Perceptual priming effects without response association were larger than semantic priming effects without response association. Furthermore, the P2 component and the P3(b) component were modulated through perceptual congruency. Semantic congruency was reflected in an N400-like effect with a delayed latency. Perceptual ERP effects were observed earlier and with different distributions than semantic ERP effects. Perceptual and semantic priming effects seem to be based on different mechanisms that share several attributes. However, the current work supports the idea of approaching consciousness through the comparison of different masking methods (cf. Breitmeyer, 2014)

Neurophysiological assessments of low-level and high-level interdependencies between auditory and visual systems in the human brain

This dissertation investigates the functional interplay between visual and auditory systems and its degree of experience-dependent plasticity. To function efficiently in everyday life, we must rely on our senses, building complex hierarchical representations about the environment. Early sensory deprivation, congenital (from birth) or within the first year of life, is a key model to study sensory experience and the degree of compensatory reorganizations (i.e., neuroplasticity). Neuroplasticity can be intramodal (within the sensory system) and crossmodal (the recruitment of deprived cortical areas for remaining senses). However, the exact role of early sensory experience and the mechanisms guiding experience-driven plasticity need further investigation. To this aim, we performed three electroencephalographic studies, considering the aspects: 1) sensory modality (auditory/visual), 2) hierarchy of the brain functional organization (low-/high-level), and 3)sensory deprivation (deprived/non-deprived cortices). The first study explored how early auditory experience affects low-level visual processing, using time-frequency analysis on the data of early deaf individuals and their hearing counterparts. The second study investigated experience- dependent plasticity in hierarchically organized face processing, applying fast periodic visual stimulation in congenitally deaf signers and their hearing controls. The third study assessed neural responses of blindfolded participants, using naturalistic stimuli together with temporal response function, and evaluated neural tracking in hierarchically organized speech processing when retinal input is absent, focusing on the role of the visual cortex. The results demonstrate the importance of atypical early sensory experience in shaping (via intra-and crossmodal changes) the brain organization at various hierarchical stages of sensory processing but also support the idea that some crossmodal effects emerge even with typical experience. This dissertation provides new insights into understanding the functional interplay between visual and auditory systems and the related mechanisms driving experience-dependent plasticity and may contribute to the development of sensory restoration tools and rehabilitation strategies for sensory-typical and sensory-deprived populations