Temporal fluctuations in the brain's modular architecture during movie-watching.
Ontology highlight
ABSTRACT:
SUBMITTER: Betzel RF
PROVIDER: S-EPMC7165071 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:BackgroundA well-characterized amygdala-dorsomedial prefrontal circuit is thought to be crucial for threat vigilance during anxiety. However, engagement of this circuitry within relatively naturalistic paradigms remains unresolved.MethodsUsing an open functional magnetic resonance imaging dataset (Cambridge Centre for Ageing Neuroscience; n = 630), we sought to investigate whether anxiety correlates with dynamic connectivity between the amygdala and dorsomedial prefrontal cortex during movie watching.ResultsUsing an intersubject representational similarity approach, we saw no effect of anxiety when comparing pairwise similarities of dynamic connectivity across the entire movie. However, preregistered analyses demonstrated a relationship between anxiety, amygdala-prefrontal dynamics, and anxiogenic features of the movie (canonical suspense ratings). Our results indicated that amygdala-prefrontal circuitry was modulated by suspense in low-anxiety individuals but was less sensitive to suspense in high-anxiety individuals. We suggest that this could also be related to slowed habituation or amplified anticipation. Moreover, a measure of threat-relevant attentional bias (accuracy/reaction time to fearful faces) demonstrated an association with connectivity and suspense.ConclusionsOverall, this study demonstrated the presence of anxiety-relevant differences in connectivity during movie watching, varying with anxiogenic features of the movie. Mechanistically, exactly how and when these differences arise remains an opportunity for future research.
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Project description:Human eye blinking is cognitively suppressed to minimize loss of visual information for important real-world events. Despite the relationship between eye blinking and cognitive state, the effect of eye blinks on cognition in real-world environments has received limited research attention. In this study, we focused on the temporal pattern of inter-eye blink interval (IEBI) during movie watching and investigated its relationship with episodic memory. As a control condition, 24 healthy subjects watched a nature documentary that lacked a specific story line while electroencephalography was performed. Immediately after viewing the movie, the subjects were asked to report its most memorable scene. Four weeks later, subjects were asked to score 32 randomly selected scenes from the movie, based on how much they were able to remember and describe. The results showed that the average IEBI was significantly longer during the movie than in the control condition. In addition, the significant increase in IEBI when watching a movie coincided with the most memorable scenes of the movie. The results suggested that the interesting episodic narrative of the movie attracted the subjects' visual attention relative to the documentary clip that did not have a story line. In the episodic memory test executed four weeks later, memory performance was significantly positively correlated with IEBI (p<0.001). In summary, IEBI may be a reliable bio-marker of the degree of concentration on naturalistic content that requires visual attention, such as a movie.
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Project description:To refine our understanding of autism spectrum disorders (ASD), studies of the brain in dynamic, multimodal and ecological experimental settings are required. One way to achieve this is to compare the neural responses of ASD and typically developing (TD) individuals when viewing a naturalistic movie, but the temporal complexity of the stimulus hampers this task, and the presence of intrinsic functional connectivity (FC) may overshadow movie-driven fluctuations. Here, we detected inter-subject functional correlation (ISFC) transients to disentangle movie-induced functional changes from underlying resting-state activity while probing FC dynamically. When considering the number of significant ISFC excursions triggered by the movie across the brain, connections between remote functional modules were more heterogeneously engaged in the ASD population. Dynamically tracking the temporal profiles of those ISFC changes and tying them to specific movie subparts, this idiosyncrasy in ASD responses was then shown to involve functional integration and segregation mechanisms such as response inhibition, background suppression, or multisensory integration, while low-level visual processing was spared. Through the application of a new framework for the study of dynamic experimental paradigms, our results reveal a temporally localized idiosyncrasy in ASD responses, specific to short-lived episodes of long-range functional interplays.
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Project description:BOLD fMRI studies have provided compelling evidence that the human brain demonstrates substantial moment-to-moment fluctuations in both activity and functional connectivity (FC) patterns. While the role of brain signal variability in fostering cognitive adaptation to ongoing environmental demands is well-documented, the relevance of moment-to-moment changes in FC patterns is still debated. Here, we adopt a graph theoretical approach in order to shed light on the cognitive-affective implications of FC variability and associated profiles of functional network communication in adulthood. Our goal is to identify brain communication pathways underlying FC reconfiguration at multiple timescales, thereby improving understanding of how faster perceptually bound versus slower conceptual processes shape neural tuning to the dynamics of the external world and, thus, indirectly, mold affective and cognitive responding to the environment. To this end, we used neuroimaging and behavioural data collected during movie watching by the Cambridge Center for Ageing and Neuroscience (N = 642, 326 women) and the Human Connectome Project (N = 176, 106 women). FC variability evoked by changes to both the concrete perceptual and the more abstract conceptual representation of an ongoing situation increased from young to older adulthood. However, coupling between variability in FC patterns and concrete environmental features was stronger at younger ages. FC variability (both moment-to-moment/concrete featural and abstract conceptual boundary-evoked) was associated with age-distinct profiles of network communication, specifically, greater functional integration of the default mode network in older adulthood, but greater informational flow across neural networks implicated in environmentally driven attention and control (cingulo-opercular, salience, ventral attention) in younger adulthood. Whole-brain communication pathways anchored in default mode regions relevant to episodic and semantic context creation (i.e., angular and middle temporal gyri) supported FC reconfiguration in response to changes in the conceptual representation of an ongoing situation (i.e., narrative event boundaries), as well as stronger coupling between moment-to-moment fluctuations in FC and concrete environmental features. Fluid intelligence/abstract reasoning was directly linked to levels of brain-environment alignment, but only indirectly associated with levels of FC variability. Specifically, stronger coupling between moment-to-moment FC variability and concrete environmental features predicted poorer fluid intelligence and greater affectively driven environmental vigilance. Complementarily, across the adult lifespan, higher fluid (but not crystallised) intelligence was related to stronger expression of the network communication profile underlying momentary and event boundary-based FC variability during youth. Our results indicate that the adaptiveness of dynamic FC reconfiguration during naturalistic information processing changes across the lifespan due to the associated network communication profiles. Moreover, our findings on brain-environment alignment complement the existing literature on the beneficial consequences of modulating brain signal variability in response to environmental complexity. Specifically, they imply that coupling between moment-to-moment FC variability and concrete environmental features may index a bias towards perceptually-bound, rather than conceptual processing, which hinders affective functioning and strategic cognitive engagement with the external environment.
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Project description:The extensive development of graph-theoretic analysis for functional connectivity has revealed the multifaceted characteristics of brain networks. Network centralities identify the principal functional regions, individual differences, and hub structure in brain networks. Neuroimaging studies using movie-watching have investigated brain function under naturalistic stimuli. Visual saliency is one of the promising measures for revealing cognition and emotions driven by naturalistic stimuli. This study investigated whether the visual saliency in movies was associated with network centrality. The study examined eigenvector centrality (EC), which is a measure of a region's influence in the brain network, and the participation coefficient (PC), which reflects the hub structure in the brain, was used for comparison. Static and time-varying EC and PC were analyzed by a parcel-based technique. While EC was correlated with brain activity in parcels in the visual and auditory areas during movie-watching, it was only correlated with parcels in the visual areas in the retinotopy task. In addition, high PC was consistently observed in parcels in the putative hub both during the tasks and the resting-state condition. Time-varying EC in the parietal parcels and time-varying PC in the primary sensory parcels significantly correlated with visual saliency in the movies. These results suggest that time-varying centralities in brain networks are distinctively associated with perceptual processing and subsequent higher processing of visual saliency.
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Project description:A fundamental question in systems neuroscience is how endogenous neuronal activity self-organizes during particular brain states. Recent neuroimaging studies have demonstrated systematic relationships between resting-state and task-induced functional connectivity (FC). In particular, continuous task studies, such as movie watching, speak to alterations in coupling among cortical regions and enhanced fluctuations in FC compared to the resting-state. This suggests that FC may reflect systematic and large-scale reorganization of functionally integrated responses while subjects are watching movies. In this study, we characterized fluctuations in FC during resting-state and movie-watching conditions. We found that the FC patterns induced systematically by movie-watching can be explained with a single principal component. These condition-specific FC fluctuations overlapped with inter-subject synchronization patterns in occipital and temporal brain regions. However, unlike inter-subject synchronization, condition-specific FC patterns were characterized by increased correlations within frontal brain regions and reduced correlations between frontal-parietal brain regions. We investigated these condition-specific functional variations as a shorter time scale, using time-resolved FC. The time-resolved FC showed condition-specificity over time; notably when subjects watched both the same and different movies. To explain self-organisation of global FC through the alterations in local dynamics, we used a large-scale computational model. We found that condition-specific reorganization of FC could be explained by local changes that engendered changes in FC among higher-order association regions, mainly in frontal and parietal cortices.
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