Spatiotemporal Brain Dynamics Research Articles

Impaired brain ability of older adults to transit and persist to latent states with well-organized structures at wakeful rest.

The intrinsic brain functional network organization continuously changes with aging. By integrating spatial and temporal information, the process of how brain networks temporally reconfigure and remain well-organized spatial structure largely reflects the brain function, thereby holds the potential to capture its age-related declines. In this study, we examined the spatiotemporal brain dynamics from resting-state functional Magnetic Resonance Imaging (fMRI) data of healthy young and older adults using a Hidden Markov Model (HMM). Six brain states were generated by HMM, with the young group showing higher fractional occupancy and mean dwell time in states 1, 3, and 4 (SY1, SY2 and SY3), and the older group in states 2, 5, and 6 (SO1, SO2 and SO3). Importantly, comparisons of transition probabilities revealed that the older group showed a reduced brain ability to transition into states dominated by the younger group, as well as a diminished capacity to persist in them. Moreover, graph analysis revealed that these young-specific states exhibited higher modularity and k-coreness. Collectively, these findings suggested that the older group showed impaired brain ability of both transition into and sustain well spatially organized states. This emphasized that the temporal changes in brain state organization, rather than its static mode, could be a key biomarker for detecting age-related functional decline. These insights may pave the way for targeted interventions aimed at mitigating cognitive decline in the aging population.

Intentional binding for noninvasive BCI control.

Noninvasive brain-computer interfaces (BCIs) allow to interact with the external environment by naturally bypassing the musculoskeletal system.
Making BCIs efficient and accurate is paramount to improve the reliability of real-life and clinical applications, from open-loop device control to closed-loop neurorehabilitation. By promoting sense of agency and embodiment, realistic setups including multimodal channels of communication, such as eye-gaze, and robotic prostheses aim to improve BCI performance. However, how the mental imagery command should be integrated in those hybrid systems so as to ensure the best interaction is still poorly understood.
To address this question, we performed a hybrid EEG-based BCI training involving healthy volunteers enrolled in a reach-and-grasp action operated by a robotic arm. Main results showed that the hand grasping motor imagery timing significantly affects the BCI accuracy evolution as well as the spatiotemporal brain dynamics. Larger accuracy improvement was obtained when motor imagery is performed just after the robot reaching, as compared to before or during the movement. The proximity with the subsequent robot grasping favored intentional binding, led to stronger motor-related brain activity, and primed the ability of sensorimotor areas to integrate information from regions implicated in higher-order cognitive functions.
Taken together, these findings provided fresh evidence about the effects of intentional binding on human behavior and cortical network dynamics that can be exploited to design a new generation of efficient brain-machine interfaces.

Differences in spatiotemporal brain network dynamics of Montessori and traditionally schooled students

Across development, experience has a strong impact on the way we think and adapt. School experience affects academic and social-emotional outcomes, yet whether differences in pedagogical experience modulate underlying brain network development is still unknown. In this study, we compared the brain network dynamics of students with different pedagogical backgrounds. Specifically, we characterized the diversity and stability of brain activity at rest by combining both resting-state fMRI and diffusion-weighted structural imaging data of 87 4–18 years old students experiencing either the Montessori pedagogy (i.e., student-led, trial-and-error pedagogy) or the traditional pedagogy (i.e., teacher-led, test-based pedagogy). Our results revealed spatiotemporal brain dynamics differences between students as a function of schooling experience at the whole-brain level. Students from Montessori schools showed overall higher functional integration (higher system diversity) and neural stability (lower spatiotemporal diversity) compared to traditionally schooled students. Higher integration was explained mainly through the cerebellar (CBL) functional network. In contrast, higher temporal stability was observed in the ventral attention, dorsal attention, somatomotor, frontoparietal, and CBL functional networks. This study suggests a form of experience-dependent dynamic functional connectivity plasticity, in learning-related networks.

Learning Spatiotemporal Brain Dynamics in Adolescents via Multimodal MEG and fMRI Data Fusion Using Joint Tensor/Matrix Decomposition.

Brain function is understood to be regulated by complex spatiotemporal dynamics, and can be characterized by a combination of observed brain response patterns in time and space. Magnetoencephalography (MEG), with its high temporal resolution, and functional magnetic resonance imaging (fMRI), with its high spatial resolution, are complementary imaging techniques with great potential to reveal information about spatiotemporal brain dynamics. Hence, the complementary nature of these imaging techniques holds much promise to study brain function in time and space, especially when the two data types are allowed to fully interact. We employed coupled tensor/matrix factorization (CMTF) to extract joint latent components in the form of unique spatiotemporal brain patterns that can be used to study brain development and function on a millisecond scale. Using the CMTF model, we extracted distinct brain patterns that revealed fine-grained spatiotemporal brain dynamics and typical sensory processing pathways informative of high-level cognitive functions in healthy adolescents. The components extracted from multimodal tensor fusion possessed better discriminative ability between high- and low-performance subjects than single-modality data-driven models. Multimodal tensor fusion successfully identified spatiotemporal brain dynamics of brain function and produced unique components with high discriminatory power. The CMTF model is a promising tool for high-order, multimodal data fusion that exploits the functional resolution of MEG and fMRI, and provides a comprehensive picture of the developing brain in time and space.

Revealing the spatiotemporal brain dynamics of covert speech compared with overt speech: A simultaneous EEG-fMRI study

Covert speech (CS) refers to speaking internally to oneself without producing any sound or movement. CS is involved in multiple cognitive functions and disorders. Reconstructing CS content by brain-computer interface (BCI) is also an emerging technique. However, it is still controversial whether CS is a truncated neural process of overt speech (OS) or involves independent patterns. Here, we performed a word-speaking experiment with simultaneous EEG-fMRI. It involved 32 participants, who generated words both overtly and covertly. By integrating spatial constraints from fMRI into EEG source localization, we precisely estimated the spatiotemporal dynamics of neural activity. During CS, EEG source activity was localized in three regions: the left precentral gyrus, the left supplementary motor area, and the left putamen. Although OS involved more brain regions with stronger activations, CS was characterized by an earlier event-locked activation in the left putamen (peak at 262 ms versus 1170 ms). The left putamen was also identified as the only hub node within the functional connectivity (FC) networks of both OS and CS, while showing weaker FC strength towards speech-related regions in the dominant hemisphere during CS. Path analysis revealed significant multivariate associations, indicating an indirect association between the earlier activation in the left putamen and CS, which was mediated by reduced FC towards speech-related regions. These findings revealed the specific spatiotemporal dynamics of CS, offering insights into CS mechanisms that are potentially relevant for future treatment of self-regulation deficits, speech disorders, and development of BCI speech applications.

Brain dynamics predictive of response to psilocybin for treatment-resistant depression.

Psilocybin therapy for depression has started to show promise, yet the underlying causal mechanisms are not currently known. Here, we leveraged the differential outcome in responders and non-responders to psilocybin (10 and 25 mg, 7 days apart) therapy for depression-to gain new insights into regions and networks implicated in the restoration of healthy brain dynamics. We used large-scale brain modelling to fit the spatiotemporal brain dynamics at rest in both responders and non-responders before treatment. Dynamic sensitivity analysis of systematic perturbation of these models enabled us to identify specific brain regions implicated in a transition from a depressive brain state to a healthy one. Binarizing the sample into treatment responders (>50% reduction in depressive symptoms) versus non-responders enabled us to identify a subset of regions implicated in this change. Interestingly, these regions correlate with in vivo density maps of serotonin receptors 5-hydroxytryptamine 2a and 5-hydroxytryptamine 1a, which psilocin, the active metabolite of psilocybin, has an appreciable affinity for, and where it acts as a full-to-partial agonist. Serotonergic transmission has long been associated with depression, and our findings provide causal mechanistic evidence for the role of brain regions in the recovery from depression via psilocybin.

Phase-encoded fMRI tracks down brainstorms of natural language processing with subsecond precision.

Natural language processing unfolds information overtime as spatially separated, multimodal, and interconnected neural processes. Existing noninvasive subtraction-based neuroimaging techniques cannot simultaneously achieve the spatial and temporal resolutions required to visualize ongoing information flows across the whole brain. Here we have developed rapid phase-encoded designs to fully exploit the temporal information latent in functional magnetic resonance imaging data, as well as overcoming scanner noise and head-motion challenges during overt language tasks. We captured real-time information flows as coherent hemodynamic waves traveling over the cortical surface during listening, reading aloud, reciting, and oral cross-language interpreting tasks. We were able to observe the timing, location, direction, and surge of traveling waves in all language tasks, which were visualized as "brainstorms" on brain "weather" maps. The paths of hemodynamic traveling waves provide direct evidence for dual-stream models of the visual and auditory systems as well as logistics models for crossmodal and cross-language processing. Specifically, we have tracked down the step-by-step processing of written or spoken sentences first being received and processed by the visual or auditory streams, carried across language and domain-general cognitive regions, and finally delivered as overt speeches monitored through the auditory cortex, which gives a complete picture of information flows across the brain during natural language functioning. PRACTITIONER POINTS: Phase-encoded fMRI enables simultaneous imaging of high spatial and temporal resolution, capturing continuous spatiotemporal dynamics of the entire brain during real-time overt natural language tasks. Spatiotemporal traveling wave patterns provide direct evidence for constructing comprehensive and explicit models of human information processing. This study unlocks the potential of applying rapid phase-encoded fMRI to indirectly track the underlying neural information flows of sequential sensory, motor, and high-order cognitive processes.

Brain microstate spatio-temporal dynamics as a candidate endotype of consciousness

Consciousness can be defined as a phenomenological experience continuously evolving. Current research showed how conscious mental activity can be subdivided into a series of atomic brain states converging to a discrete spatiotemporal pattern of global neuronal firing. Using the high temporal resolution of EEG recordings in patients with a severe Acquired Brain Injury (sABI) admitted to an Intensive Rehabilitation Unit (IRU), we detected a novel endotype of consciousness from the spatiotemporal brain dynamics identified via microstate analysis. Also, we investigated whether microstate features were associated with common neurophysiological alterations. Finally, the prognostic information comprised in such descriptors was analysed in a sub-cohort of patients with prolonged Disorder of Consciousness (pDoC). Occurrence of frontally-oriented microstates (C microstate), likelihood of maintaining such brain state or transitioning to the C topography and complexity were found to be indicators of consciousness presence and levels. Features of left–right asymmetric microstates and transitions toward them were found to be negatively correlated with antero-posterior brain reorganization and EEG symmetry. Substantial differences in microstates’ sequence complexity and presence of C topography were found between groups of patients with alpha dominant background, cortical reactivity and antero-posterior gradient. Also, transitioning from left-right to antero-posterior microstates was found to be an independent predictor of consciousness recovery, stronger than consciousness levels at IRU’s admission. In conclusions, global brain dynamics measured with scale-free estimators can be considered an indicator of consciousness presence and a candidate marker of short-term recovery in patients with a pDoC.

Posterior theta activity reveals an early signal of self-face recognition

Self-related visual information, especially one’s own face and name, are processed in a specific, prioritized way. However, the spatio-temporal brain dynamics of self-prioritization have remained elusive. Moreover, it has been unclear whether this prioritization is an effect of enhancement and amplification, or rather a facilitating automatization of processing self-referential information. In this EEG study, 25 married women (who changed their surnames after marriage, so that their past and present surnames could be used as stimuli) performed a detection task with faces and names from five categories: self, self from the past, friend, famous, and unknown person. The aim was to determine the temporal and spatial characteristics of early electrophysiological markers of self-referential processing. We report results of event-related component (ERP) and time–frequency analyses. In the ERPs, the earliest self-relevance effect was displayed only 300 ms after stimulus onset in the midfrontal N2, and later in the parietal P3b, independently of the stimulus type. No self-relevance effect was found on the N170 component. However, local theta power at the occipito-temporal (visual) areas and inter-regional theta phase coherence between the visual and midfrontal areas showed that self-relevance differentiation of faces began already about 100–300 ms after stimulus onset. No such early effects were found for names. The results are discussed in terms of the time-course, functional localization, stimulus-specificity, and automatization of self-prioritization.

Prediction and detection of virtual reality induced cybersickness: a spiking neural network approach using spatiotemporal EEG brain data and heart rate variability

Virtual Reality (VR) allows users to interact with 3D immersive environments and has the potential to be a key technology across many domain applications, including access to a future metaverse. Yet, consumer adoption of VR technology is limited by cybersickness (CS)—a debilitating sensation accompanied by a cluster of symptoms, including nausea, oculomotor issues and dizziness. A leading problem is the lack of automated objective tools to predict or detect CS in individuals, which can then be used for resistance training, timely warning systems or clinical intervention. This paper explores the spatiotemporal brain dynamics and heart rate variability involved in cybersickness and uses this information to both predict and detect CS episodes. The present study applies deep learning of EEG in a spiking neural network (SNN) architecture to predict CS prior to using VR (85.9%, F7) and detect it (76.6%, FP1, Cz). ECG-derived sympathetic heart rate variability (HRV) parameters can be used for both prediction (74.2%) and detection (72.6%) but at a lower accuracy than EEG. Multimodal data fusion of EEG and sympathetic HRV does not change this accuracy compared to ECG alone. The study found that Cz (premotor and supplementary motor cortex) and O2 (primary visual cortex) are key hubs in functionally connected networks associated with both CS events and susceptibility to CS. F7 is also suggested as a key area involved in integrating information and implementing responses to incongruent environments that induce cybersickness. Consequently, Cz, O2 and F7 are presented here as promising targets for intervention.

Interacting spiral wave patterns underlie complex brain dynamics and are related to cognitive processing.

The large-scale activity of the human brain exhibits rich and complex patterns, but the spatiotemporal dynamics of these patterns and their functional roles in cognition remain unclear. Here by characterizing moment-by-moment fluctuations of human cortical functional magnetic resonance imaging signals, we show that spiral-like, rotational wave patterns (brain spirals) are widespread during both resting and cognitive task states. These brain spirals propagate across the cortex while rotating around their phase singularity centres, giving rise to spatiotemporal activity dynamics with non-stationary features. The properties of these brain spirals, such as their rotational directions and locations, are task relevant and can be used to classify different cognitive tasks. We also demonstrate that multiple, interacting brain spirals are involved in coordinating the correlated activations and de-activations of distributed functional regions; this mechanism enables flexible reconfiguration of task-driven activity flow between bottom-up and top-down directions during cognitive processing. Our findings suggest that brain spirals organize complex spatiotemporal dynamics of the human brain and have functional correlates to cognitive processing.

Brain responses to food viewing in women during pregnancy and post partum and their relationship with metabolic health: study protocol for the FOODY Brain Study, a prospective observational study

IntroductionFood cravings are common in pregnancy and along with emotional eating and eating in the absence of hunger, they are associated with excessive weight gain and adverse effects on metabolic...

Ordinal methods for a characterization of evolving functional brain networks.

Ordinal time series analysis is based on the idea to map time series to ordinal patterns, i.e., order relations between the values of a time series and not the values themselves, as introduced in 2002 by C. Bandt and B. Pompe. Despite a resulting loss of information, this approach captures meaningful information about the temporal structure of the underlying system dynamics as well as about properties of interactions between coupled systems. This-together with its conceptual simplicity and robustness against measurement noise-makes ordinal time series analysis well suited to improve characterization of the still poorly understood spatiotemporal dynamics of the human brain. This minireview briefly summarizes the state-of-the-art of uni- and bivariate ordinal time-series-analysis techniques together with applications in the neurosciences. It will highlight current limitations to stimulate further developments, which would be necessary to advance characterization of evolving functional brain networks.

Data-driven discovery of canonical large-scale brain dynamics.

Human behavior and cognitive function correlate with complex patterns of spatio-temporal brain dynamics, which can be simulated using computational models with different degrees of biophysical realism. We used a data-driven optimization algorithm to determine and classify the types of local dynamics that enable the reproduction of different observables derived from functional magnetic resonance recordings. The phase space analysis of the resulting equations revealed a predominance of stable spiral attractors, which optimized the similarity to the empirical data in terms of the synchronization, metastability, and functional connectivity dynamics. For stable limit cycles, departures from harmonic oscillations improved the fit in terms of functional connectivity dynamics. Eigenvalue analyses showed that proximity to a bifurcation improved the accuracy of the simulation for wakefulness, whereas deep sleep was associated with increased stability. Our results provide testable predictions that constrain the landscape of suitable biophysical models, while supporting noise-driven dynamics close to a bifurcation as a canonical mechanism underlying the complex fluctuations that characterize endogenous brain activity.

Deep neural networks constrained by neural mass models improve electrophysiological source imaging of spatiotemporal brain dynamics

Many efforts have been made to image the spatiotemporal electrical activity of the brain with the purpose of mapping its function and dysfunction as well as aiding the management of brain disorders. Here, we propose a non-conventional deep learning-based source imaging framework (DeepSIF) that provides robust and precise spatiotemporal estimates of underlying brain dynamics from noninvasive high-density electroencephalography (EEG) recordings. DeepSIF employs synthetic training data generated by biophysical models capable of modeling mesoscale brain dynamics. The rich characteristics of underlying brain sources are embedded in the realistic training data and implicitly learned by DeepSIF networks, avoiding complications associated with explicitly formulating and tuning priors in an optimization problem, as often is the case in conventional source imaging approaches. The performance of DeepSIF is evaluated by 1) a series of numerical experiments, 2) imaging sensory and cognitive brain responses in a total of 20 healthy subjects from three public datasets, and 3) rigorously validating DeepSIF's capability in identifying epileptogenic regions in a cohort of 20 drug-resistant epilepsy patients by comparing DeepSIF results with invasive measurements and surgical resection outcomes. DeepSIF demonstrates robust and excellent performance, producing results that are concordant with common neuroscience knowledge about sensory and cognitive information processing as well as clinical findings about the location and extent of the epileptogenic tissue and outperforming conventional source imaging methods. The DeepSIF method, as a data-driven imaging framework, enables efficient and effective high-resolution functional imaging of spatiotemporal brain dynamics, suggesting its wide applicability and value to neuroscience research and clinical applications.

A 5D approach to study spatio-temporal dynamism of resting-state brain networks in schizophrenia.

Schizophrenia is a serious brain disorder that can affect all aspects of patient's life such as thinking, behaving and even feeling. The principal cause of schizophrenia is still unknown, but there is some evidence that differences in brain networks interactions along with functional dysconnectivity may play a significant role. Prior work has mostly focused on static summaries of functional data, or more recently changes in temporal coupling between fixed networks. Here, we study differences in spatio-temporal brain dynamics using resting state fMRI images in a dataset including 510 control and 708 schizophrenia patients. To do this, we utilized a deep residual network to extract 5 different spatiotemporal networks each of which captures spatial and temporal dynamics within sensory-motor, auditory, and default mode domains. Our analysis shows significant group differences in various aspects of spatio-temporal dynamics including magnitude, voxel-wise variability, and temporal functional network connectivity. Clinical relevance- Our study explores effects of spatio-temporal brain dynamism in schizophrenia, which is rarely taken into account, but could provide unique and more sensitive information about the disorder. Here we incorporate a novel 5D brain parcellation model, that enables us to encode spatio-temporal dynamics, to extract and characterize multiple resting fMRI brain networks.

Forecasting brain activity based on models of spatiotemporal brain dynamics: A comparison of graph neural network architectures.

Comprehending the interplay between spatial and temporal characteristics of neural dynamics can contribute to our understanding of information processing in the human brain. Graph neural networks (GNNs) provide a new possibility to interpret graph-structured signals like those observed in complex brain networks. In our study we compare different spatiotemporal GNN architectures and study their ability to model neural activity distributions obtained in functional MRI (fMRI) studies. We evaluate the performance of the GNN models on a variety of scenarios in MRI studies and also compare it to a VAR model, which is currently often used for directed functional connectivity analysis. We show that by learning localized functional interactions on the anatomical substrate, GNN-based approaches are able to robustly scale to large network studies, even when available data are scarce. By including anatomical connectivity as the physical substrate for information propagation, such GNNs also provide a multimodal perspective on directed connectivity analysis, offering a novel possibility to investigate the spatiotemporal dynamics in brain networks.

Spatio-temporal brain dynamics of self-identity: an EEG source analysis of the current and past self

Current research on self-identity suggests that the self is settled in a unique mental representation updated across the lifespan in autobiographical memory. Spatio-temporal brain dynamics of these cognitive processes are poorly understood. ERP studies revealed early (N170-N250) and late (P3-LPC) waveforms modulations tracking the temporal processing of global face configuration, familiarity processes, and access to autobiographical contents. Neuroimaging studies revealed that such processes encompass face-specific regions of the occipitotemporal cortex, and medial cortical regions tracing the self-identity into autobiographical memory across the life span. The present study combined both approaches, analyzing brain source power using a data-driven, beamforming approach. Face recognition was used in two separate tasks: identity (self, close friend and unknown) and life stages (childhood, adolescence, adulthood) recognition. The main areas observed were specific-face areas (fusiform area), autobiographical memory areas (medial prefrontal cortex, parahippocampus, posterior cingulate cortex/precuneus), along with executive areas (dorsolateral prefrontal and anterior temporal cortices). The cluster-permutation test yielded no significant early effects (150–200 ms). However, during the 250–300 ms time window, the precuneus and the fusiform cortices exhibited larger activation to familiar compared to unknown faces, regardless of life stages. Subsequently (300–600 ms), the medial prefrontal cortex discriminates between self-identity vs. close-familiar and unknown. Moreover, significant effects were found in the cluster-permutation test specifically on self-identity discriminating between adulthood from adolescence and childhood. These findings suggest that recognizing self-identity from other facial identities (diachronic self) comprises the temporal coordination of anterior and posterior areas. While mPFC maintained an updated representation of self-identity (diachronic self) based on actual rewarding value, the dlPFC, FG, MTG, paraHC, PCC was sensitive to different life stages of self-identity (synchronic self) during the access to autobiographical memory.

Task modulation of spatiotemporal dynamics in semantic brain networks: An EEG/MEG study

How does brain activity in distributed semantic brain networks evolve over time, and how do these regions interact to retrieve the meaning of words? We compared spatiotemporal brain dynamics between visual lexical and semantic decision tasks (LD and SD), analysing whole-cortex evoked responses and spectral functional connectivity (coherence) in source-estimated electroencephalography and magnetoencephalography (EEG and MEG) recordings. Our evoked analysis revealed generally larger activation for SD compared to LD, starting in primary visual area (PVA) and angular gyrus (AG), followed by left posterior temporal cortex (PTC) and left anterior temporal lobe (ATL). The earliest activation effects in ATL were significantly left-lateralised. Our functional connectivity results showed significant connectivity between left and right ATL, PTC and right ATL in an early time window, as well as between left ATL and IFG in a later time window. The connectivity of AG was comparatively sparse. We quantified the limited spatial resolution of our source estimates via a leakage index for careful interpretation of our results. Our findings suggest that the different demands on semantic information retrieval in lexical and semantic decision tasks first modulate visual and attentional processes, then multimodal semantic information retrieval in the ATLs and finally control regions (PTC and IFG) in order to extract task-relevant semantic features for response selection. Whilst our evoked analysis suggests a dominance of left ATL for semantic processing, our functional connectivity analysis also revealed significant involvement of right ATL in the more demanding semantic task. Our findings demonstrate the complementarity of evoked and functional connectivity analysis, as well as the importance of dynamic information for both types of analyses.

Rapid encoding of musical tones discovered in whole-brain connectivity

Information encoding has received a wide neuroscientific attention, but the underlying rapid spatiotemporal brain dynamics remain largely unknown. Here, we investigated the rapid brain mechanisms for encoding of sounds forming a complex temporal sequence. Specifically, we used magnetoencephalography (MEG) to record the brain activity of 68 participants while they listened to a highly structured musical prelude. Functional connectivity analyses performed using phase synchronisation and graph theoretical measures showed a large network of brain areas recruited during encoding of sounds, comprising primary and secondary auditory cortices, frontal operculum, insula, hippocampus and basal ganglia. Moreover, our results highlighted the rapid transition of brain activity from primary auditory cortex to higher order association areas including insula and superior temporal pole within a whole-brain network, occurring during the first 220 ms of the encoding process. Further, we discovered that individual differences along cognitive abilities and musicianship modulated the degree centrality of the brain areas implicated in the encoding process. Indeed, participants with higher musical expertise presented a stronger centrality of superior temporal gyrus and insula, while individuals with high working memory abilities showed a stronger centrality of frontal operculum. In conclusion, our study revealed the rapid unfolding of brain network dynamics responsible for the encoding of sounds and their relationship with individual differences, showing a complex picture which extends beyond the well-known involvement of auditory areas. Indeed, our results expanded our understanding of the general mechanisms underlying auditory pattern encoding in the human brain.