Age and sex affect intersubject correlation of EEG throught development

Recent efforts have aimed to characterize clinical pediatric populations by using neurophysiological tests in addition to behavioral assays. Here we report on a data collection effort in which electroencephalography (EEG) was recorded in both juveniles and adults (N=114 participants, ages 6-44 years of age) during various stimulation protocols. The present analysis focuses on how neural responses during passive viewing of naturalistic videos vary with age and sex, and in particular, how similar they are within developmental groups. Similarity of neural responses was measured as the inter-subject correlation of the EEG. Stimulus-evoked neural responses are more similar among children and decrease in similarity with age. Among children, males respond more similarly to each other than females. This was uniformly true for a variety of videos. The decrease in group similarity with age may result from an overall decline in the magnitude of evoked responses, but this cannot explain the sex differences found in the young. We therefore propose that as children mature, neural function may become more variable

Aberrant Cortical Integration in First-Episode Psychosis During Natural Audiovisual Processing

BACKGROUND: Functional magnetic resonance imaging studies of psychotic disorders have reported both hypoactivity and hyperactivity in numerous brain regions. In line with the dysconnection hypothesis, these regions include cortical integrative hub regions. However, most earlier studies focused on a single cognitive function at a time, assessed by delivering artificial stimuli to patients with chronic psychosis. Thus, it remains unresolved whether these findings are present already in early psychosis and whether they translate to real-life-like conditions that require multisensory processing and integration. METHODS: Scenes from the movie Alice in Wonderland (2010) were shown to 51 patients with first-episode psychosis (16 women) and 32 community-based control subjects (17 women) during 3T functional magnetic resonance imaging. We compared intersubject correlation, a measure of similarity of brain signal time courses in each voxel, between the groups. We also quantified the hubness as the number of connections each region has. RESULTS: Intersubject correlation was significantly lower in patients with first-episode psychosis than in control subjects in the medial and lateral prefrontal, cingulate, precuneal, and parietotemporal regions, including the default mode network. Regional magnitude of between-group difference in intersubject correlation was associated with the hubness. CONCLUSIONS: Our findings provide novel evidence for the dysconnection hypothesis by showing that during complex real-life-like stimulation, the most prominent functional alterations in psychotic disorders relate to integrative brain functions. Presence of such abnormalities in first-episode psychosis rules out long-term effects of illness or medication. These methods can be used in further studies to map widespread hub alterations in a single functional magnetic resonance imaging session and link them to potential downstream and upstream pathways.Peer reviewe

The “Narratives” fMRI dataset for evaluating models of naturalistic language comprehension

The “Narratives” collection aggregates a variety of functional MRI datasets collected while human subjects listened to naturalistic spoken stories. The current release includes 345 subjects, 891 functional scans, and 27 diverse stories of varying duration totaling ~4.6 hours of unique stimuli (~43,000 words). This data collection is well-suited for naturalistic neuroimaging analysis, and is intended to serve as a benchmark for models of language and narrative comprehension. We provide standardized MRI data accompanied by rich metadata, preprocessed versions of the data ready for immediate use, and the spoken story stimuli with time-stamped phoneme- and word-level transcripts. All code and data are publicly available with full provenance in keeping with current best practices in transparent and reproducible neuroimaging

Loss of reliable temporal structure in event-related averaging of naturalistic stimuli

To separate neural signals from noise, brain responses measured in neuroimaging are routinely averaged across space and time. However, such procedures may obscure some properties of neural activity. Recently, multi-voxel pattern analysis methods have demonstrated that patterns of activity across voxels contain valuable information that is concealed by spatial averaging. Here we show that temporal patterns of neural activity contain information that can discriminate different stimuli, even within brain regions that show no net activation to that stimulus class. Furthermore, we find that in many brain regions, responses to natural stimuli are highly context dependent. In such cases, prototypical event-related responses do not even exist for individual stimuli, so that averaging responses to the same stimulus within different contexts may worsen the effective signal-to-noise. As a result, analysis of the temporal structures of single events can reveal aspects of neural dynamics which cannot be detected using standard event-related averaging methods

Natural stimuli and experimental setups in the study of the neural basis of social interaction

Social interaction consists of events of different modalities that unfold on a subsecond timescale and are usually influenced by all involved participants. Therefore, social interaction is difficult to be simulated in laboratory, as simple, static, and unidirectional stimuli and tasks do not cover its properties accurately enough. However, moving towards more natural experimental setups in brain imaging, e.g. in magnetoencephalography (MEG), means giving up many traditional ways of analysis, such as signal averaging on the basis of pre-classified well-controlled stimuli. Thus, in addition to developing naturalistic experimental setups, new ways are needed to analyse the data and to classify the events of interest. In this thesis, ecologically valid experimental setups for brain imaging of social interaction were developed and tested in three MEG and two behavioural experiments. Of the MEG studies, the first study presented in this thesis introduced a free-viewing paradigm for MEG and showed different responses to congruent and incongruent audiovisual stimuli in the auditory cortex. In the second MEG study auditory cortex was shown to respond differently to the anticipation of emotional and neutral sounds. The third MEG study presented a setup for simultaneous MEG measurements of two interacting persons, validating its feasibility by showing reproducible and similar auditory responses in both subjects to stimuli delivered from the two measurement sites. The two behavioural studies of this thesis concentrated on turn taking behaviour in conversation. The first of them showed that the organization of turn-taking guides the gaze of an external viewer of the conversation. The latter study demonstrated that speech is a strong inducer of behavioural entrainment as speakers mutually adapted their speaking rhythms when producing sentences with a partner.Sosiaalinen vuorovaikutus koostuu jopa alle sekunnin aikaskaalalla muuttuvista ja eri aistien kautta välittyvistä tapahtumista, joihin kaikki vuorovaikutukseen osallistujat vaikuttavat. Vuorovaikutusta on vaikea simuloida laboratorio-olosuhteissa, koska yksinkertaiset, liikkumattomat ja yksisuuntaiset ärsykkeet ja tehtävät eivät toista sen ominaisuuksia riittävän tarkasti. Luonnollisempien ärsykkeiden käyttöön siirtyminen aivokuvantamisessa, kuten magnetoenkefalografiassa (MEG) tarkoittaa luopumista etukäteen luokitelluista, helposti kontrolloitavista ärsykkeistä ja niiden perinteisistä keskiarvoistusmenetelmistä. Luonnollisia ärsykkeitä hyödyntävien koeasetelmien kehittämisen lisäksi on tilalle löydettävä uusia signaalinkäsittelymenetelmiä ja tapoja etsiä ja luokitella kiinnostavia tapahtumia jatkuvan luonnollisen ärsykevirran joukosta. Väitöskirja esittelee luonnonmukaisia koeasetelmia sosiaalisen vuorovaikutuksen aivomekanismien tutkimiseen kolmessa MEG- ja kahdessa käyttäytymistutkimuksessa. MEG-tutkimuksista ensimmäisessä kuvattiin vapaan katselun mahdollistava koeasetelma ja osoitettiin sitä käyttäen yhdenmukaisten audiovisuaalisten ärsykkeiden aiheuttavan voimakkaampia kuulovasteita kuin epäyhdenmukaisten ärsykkeiden. Toinen MEG-tutkimus käsitteli kuulovasteita tunteita herättäviin luonnollisiin ääniärsykkeisiin ja osoitti neutraalien äänien herättämien vasteiden eroavan tunteita herättävien äänten aiheuttamista kuulovasteista jo ääntä odotettaessa. MEG-tutkimuksista kolmas esitteli kahden vuorovaikutuksessa olevan henkilön samanaikaiseen tutkimiseen soveltuvan MEG-järjestelmän ja osoitti sen toimivuuden molemmilta koehenkilöiltä mitatuilla toistettavilla ja yhdenmukaisilla kuulovasteilla. Väitöskirjan käyttäytymistutkimukset keskittyivät keskusteluvuoronvaihtoon. Niistä ensimmäisessä katsojien havaittiin seuraavan kahden henkilön keskustelua yhtenäisesti, ja tarkemmin silloin, kun heillä oli sekä visuaalinen että auditorinen informaatio saatavillaan. Jälkimmäinen tutkimus osoitti puheen olevan vahva puherytmien yhtenäistäjä, kun koehenkilöt kertoivat tarinaa yhdessä, vuorotellen sana sanalta lauseita muodostaen

Data Descriptor: A resource for assessing information processing in the developing brain using EEG and eye tracking

We present a dataset combining electrophysiology and eye tracking intended as a resource for the investigation of information processing in the developing brain. The dataset includes high-density taskbased and task-free EEG, eye tracking, and cognitive and behavioral data collected from 126 individuals (ages: 6–44). The task battery spans both the simple/complex and passive/active dimensions to cover a range of approaches prevalent in modern cognitive neuroscience. The active task paradigms facilitate principled deconstruction of core components of task performance in the developing brain, whereas the passive paradigms permit the examination of intrinsic functional network activity during varying amounts of external stimulation. Alongside these neurophysiological data, we include an abbreviated cognitive test battery and questionnaire-based measures of psychiatric functioning. We hope that this dataset will lead to the development of novel assays of neural processes fundamental to information processing, which can be used to index healthy brain development as well as detect pathologic processes

Neural Synchrony During Naturalistic Language Perception in Listeners with Aphasia

Neural synchrony across listeners during language processing has been found to be associated with successful comprehension in neurotypical adults. At initial presentation of auditory-visual stimuli, neural responses appear to oscillate in different rhythms across brain regions. As the stimulus progresses, the time course of neural activity synchronizes across listeners, particularly in primary auditory and visual processing regions. This phenomenon, which we refer to as ‘neural entrainment,’ has been observed in neurotypical individuals attending to the same stimulus. Neural synchrony occurs due to the inherent neural response elicited by a stimulus and has been shown to be consistent across participants in specific regions when attending to the same, time-locked stimulus. In persons with aphasia, language comprehension is often impaired, resulting in differing degrees of comprehension deficits depending on the size and location of one’s lesion. One way to explain such comprehension deficits may be a lack of neural coupling across language processing regions during naturalistic comprehension, likely caused by lesion damage. The present study investigated neural synchrony among participants with aphasia compared to neurotypical controls attending to the same naturalistic stimulus. Regions that showed significant synchrony in the control group were selected as seed regions of interest and were examined further in participants with aphasia to investigate behavioral correlates. Results indicate that individuals with aphasia do not synchronize in in-tact brain regions, and there is evidence that region-specific synchrony is associated with comprehension scores particularly in right hemisphere ventral stream regions and left posterior temporal regions. The present study provides evidence that naturalistic synchrony can explain some degree of the integrity of residual regions and regional synchrony is associated with off-line comprehension ability

Shades Of Meaning: Capturing Meaningful Context-Based Variations In Neural Patterns

When cognitive psychologists and psycholinguists consider the variability that arises during the retrieval of conceptual information, this variability it is often understood to arise from the dynamic interactions between concepts and contexts. �When cognitive neuroscientists and neurolinguists think about this variability, it is typically treated as noise and discarded from the analyses. In this dissertation, we bridge these two traditions by asking: can the variability in neural patterns evoked by word meanings reflect the contextual variation that occurs during conceptual processing? We employ functional magnetic resonance imaging (fMRI) to measure, quantify, and predict brain activity during context-dependent retrieval of word meanings. Across three experiments, we test the ways in which word-evoked neural variability is influenced by the sentence context in which the word appears (Chapter 2); the current set of task demands (Chapter 3); or even undirected thoughts about other concepts (Chapter 4). Our findings indicate that not only do the neural patterns evoked by the same stimulus word vary over time, but we can predict the degree to which these patterns vary using meaningful, theoretically motivated variables. These results demonstrate that cross-context, within-concept variations in neural responses are not exclusively due to statistical noise or measurement error. Rather, the degree of a concept’s neural variability varies in a manner that accords with a context-dependent view of semantic representation. In addition, we present preliminary evidence that prefrontally-mediated cognitive control processes are involved in expression of context-appropriate neural patterns. In sum, these studies provide a novel perspective on the flexibility of word meanings and the variable brain activity patterns associated with them

The Inter-Subject Correlation of EEG in Response to Naturalistic Stimuli

Inter-subject correlation is a measure of the similarity of the brain activity of a group of people as they respond to the same naturalistic stimulus, typically a story or video, meant to simulate a real world experience. This thesis tests the hypothesis that the correlation of the brain responses of a group of people is indicative of stimulus engagement. The rationale is that the content of the stimulus drives brain activity in a consistent manner, while internal thoughts are divergent and result in uncorrelated activity. The inter-subject correlation (ISC) of neural responses have previously been assessed with fMRI, EEG, and MEG. Here, EEG will assess ISC, thereby examining the correlation of the early responses to a stimulus. Engagement has been examined previously with self-report assessments of interest. These ratings are noisy, subject to bias, and do not measure how engagement evolves over time. In this thesis, engagement is defined as a commitment to devote a scarce resource, such as attention or time, to a stimulus. In the experiment presented here, subjects were allowed limited time with the stimuli, thus forcing them to engage with the content they determined to be most compelling. This behavioral metric strongly correlated with ISC of the EEG, thus validating it as a measure of neural engagement. Interestingly, higher ISC was also indicative of a shared perception of the passage of time across subjects. This suggests that when people are engaged with a stimulus, their perception of time is also driven by that stimulus, rather than by an internal sense of time. If people are more engaged at the time of encoding, it is likely that they will better remember their experiences. Memory was therefore assessed three weeks after subjects heard salient emotional narratives. Individuals whose EEG responses during the stories correlated more strongly with their peers had stronger memories of the events in the stories. ISC was also tested as a predictor of retention in the context of online educational videos. Again, the similarity between each subject’s brain activity and that of his or her peers corresponded with memory for factual information in a subsequent test. It is possible that people with different backgrounds do not engage with the world in similar ways, and their neural responses will therefore correlate more strongly with people who are most similar to them. To address this notion, ISC was compared across the dimensions of age and gender. In a population with ages ranging from 5 - 44 years old, ISC weakens with age and is stronger in males than it is in females. This result is consistent with the idea that age and experience are marked by an increase in the repertoire of neural representations. Adults may therefore have more variable interpretations that mediate their sensory responses to stimuli. Alternatively, if ISC is truly assessing engagement in this context, the result may demonstrate that adults are less susceptible to the influence of outside stimuli since they have more powerful internal voices that distract them. Whichever the ultimate reason for this change, the gender disparity may also be related to a developmental difference because the deviation between males and females in ISC is strongest in young ages, a period when anatomical findings show that young males are less neurally mature than young females. Although ISC is implicated in fundamental processes such as engagement, memory, and development, the neural underpinnings of this signal are unclear. The spatial distribution of the EEG signal that drives ISC appears similar on the surface of the scalp across stimuli with different narrative content, and between different stimulus modalities. The similarity of the topography of correlated activity across sensory modalities may indicate that this activity is supramodal and is therefore generated by a region that is impervious to the stimulus modality. To assess ISC’s dependence on stimulus modality and stimulus type, the modulation of ISC was compared with the fMRI BOLD responses to the same stimuli. This analysis revealed that ISC is mostly modulated by sensory regions, and that the extent of the regions involved depends on the content of the stimulus. These areas, which are largely driven by immediate processing of the stimulus at a fast timescale, are therefore implicated in higher-level behaviors such as engagement and memory

The neural basis of semantic processing across comprehension contexts

Current neurobiological models of semantic cognition have been predominately derived from studies of single-words or sentences which may provide an impoverished estimate of how semantic processing occurs in real-world contexts. Studies that make use of more ecologically valid stimuli such as natural language or narratives suggest that, counter to the hub-and-spoke framework in which the anterior temporal lobe (ATL) serves as a graded hub integrating information from proximal sensorimotor spokes, the semantic system displays voxel-wise category specialization tiled across a large, distributed network. A complicating factor in reconciling these seemingly conflicting claims is the over-reliance on concrete conceptual knowledge in describing the organization of the semantic system. A recent theoretical account argues that social knowledge, like other types of semantic knowledge, is processed within the ventrolateral ATL, but this claim has not been tested using naturalistic stimuli, which better sample abstract social knowledge, including pragmatic inference. This thesis investigates the organization of the semantic system across multiple scales, from isolated words to multimodal narratives, and across multiple types of semantic conceptual knowledge, from concrete to abstract. Using comprehension of concrete words as a starting point, the first study describes a critical examination of specialization within the semantic system for taxonomic (dog – bear) and thematic (dog – leash) relations using intracranial EEG recordings from an array of depth electrodes within ATL, inferior parietal lobule (IPL), and two regions within the semantic control network, inferior frontal gyrus (IFG) and posterior middle temporal gyrus (pMTG). Moving across the context and conceptual scale to build upon this work, the second study investigated how the concrete and abstract lexical and semantic properties of single-words, akin to those that informed the hub-and-spoke model, are processed in a complex, complete narrative presented to participants during fMRI scanning. In doing so, this study enabled comparisons between prior studies of isolated words and naturalistic work, thus moving toward an integrated cross-scale account of semantic cognition. Using the same neuroimaging data, the third study extended this work to investigate how context contributes to the construction of meaning by studying how the semantic and social cognitive systems are engaged by social and pragmatic sentence-level content. This enabled a direct, naturalistic test of the claim that social knowledge is housed within the semantic system. The fourth study investigated shared processing between social and semantic systems using fMRI data collected during movie-viewing, which captures the multimodal environment in which social knowledge is exchanged. The results of these studies collectively demonstrate that the semantic and social systems are differentially engaged across the scales investigated here. Concrete conceptual relations engage one (or more) specialized hubs within the semantic system, whereas processing of naturalistic verbal and event content co-varies with activation in large brain networks. There is evidence of functional gradations within ATL that are differentially sensitive to the demands of narrative comprehension – the anterior superior temporal gyrus (i.e., dorsolateral subregion) and anterior fusiform (i.e., ventral subregion) appear to be particularly sensitive to the quantity and informativeness of external input whereas the anterior middle and inferior temporal gyri (i.e., ventrolateral subregion) appear to be engaged by internal, or endogenous, semantic processing during narrative comprehension. Engagement of this same ventrolateral subregion is observed in response to social word and sentence content, providing support for the claim that social processing is subsumed within the semantic system. Taken together, the results suggest an extension to the current neurobiological model of semantic cognition that accommodates comprehension contexts. The studies undertaken as part of this thesis build upon the existing concept-level frameworks towards a narrative-level framework of semantic cognition