scholarly journals Consistent local dynamics in the brain across sessions are revealed by whole brain modeling of resting state activity

2017 ◽  
Author(s):  
Patricio Donnelly Kehoe ◽  
Victor M. Saenger ◽  
Nina Lisofsky ◽  
Simone Kühn ◽  
Morten L. Kringelbach ◽  
...  

AbstractResting state fMRI has been the primary tool for studying the functional organization of the human brain. However, even at so-called “rest”, ongoing brain activity and its underlying physiological organization is highly dynamic and yet most of the information generated so far comes from group analysis. Here we developed an imaging-based technique capable of portraying information of local dynamics at a single-subject level reliably by using a whole-brain model that estimates a local bifurcation parameter, which reflects if a brain region presents stable, asynchronous or transitory oscillations. Using 50 longitudinal resting state sessions of one single subject and single resting state sessions from a group of 50 participants we demonstrated that individual global and local brain dynamics can be estimated consistently with respect to a reference group using only a scanning time of 15 to 20 minutes. We also showed that brain hubs are closer to a transition point between synchronous and asynchronous oscillatory dynamics and that dynamics in frontal areas have larger variations compared to other regions. Finally, we analyzed the variability and error of these dynamics and found high symmetry between hemispheres, which interestingly was reduced by adding more sessions. The framework presented here can be used to study functional brain dynamics on an individual level, opening new avenues for possible clinical applications.Bullet pointsLocal brain dynamics are consistent across scans.Four scans of five minutes each are enough to get highly reliable and consistent results.Hub areas are in a transition point between a synchronous and asynchronous regime.Variability and error of local dynamics presented high symmetry between hemispheres.

2020 ◽  
Author(s):  
Kyesam Jung ◽  
Simon B. Eickhoff ◽  
Oleksandr V. Popovych

AbstractDynamical modeling of the resting-state brain dynamics essentially relies on the empirical neuroimaging data utilized for the model derivation and validation. There is however still no standardized data processing for magnetic resonance imaging pipelines and the structural and functional connectomes involved in the models. In this study, we thus address how the parameters of diffusion-weighted data processing for structural connectivity (SC) can influence the validation results of the whole-brain mathematical models and search for the optimal parameter settings. On this way, we simulate the functional connectivity by systems of coupled oscillators, where the underlying network is constructed from the empirical SC and evaluate the performance of the models for varying parameters of data processing. For this, we introduce a set of simulation conditions including the varying number of total streamlines of the whole-brain tractography (WBT) used for extraction of SC, cortical parcellations based on functional and anatomical brain properties and distinct model fitting modalities. We observed that the graph-theoretical network properties of structural connectome can be affected by varying tractography density and strongly relate to the model performance. We explored free parameters of the considered models and found the optimal parameter configurations, where the model dynamics closely replicates the empirical data. We also found that the optimal number of the total streamlines of WBT can vary for different brain atlases. Consequently, we suggest a way how to improve the model performance based on the network properties and the optimal parameter configurations from multiple WBT conditions. Furthermore, the population of subjects can be stratified into subgroups with divergent behaviors induced by the varying number of WBT streamlines such that different recommendations can be made with respect to the data processing for individual subjects and brain parcellations.Author summaryThe human brain connectome at macro level provides an anatomical constitution of inter-regional connections through the white matter in the brain. Understanding the brain dynamics grounded on the structural architecture is one of the most studied and important topics actively debated in the neuroimaging research. However, the ground truth for the adequate processing and reconstruction of the human brain connectome in vivo is absent, which is crucial for evaluation of the results of the data-driven as well as model-based approaches to brain investigation. In this study we thus evaluate the effect of the whole-brain tractography density on the structural brain architecture by varying the number of total axonal fiber streamlines. The obtained results are validated throughout the dynamical modeling of the resting-state brain dynamics. We found that the tractography density may strongly affect the graph-theoretical network properties of the structural connectome. The obtained results also show that a dense whole-brain tractography is not always the best condition for the modeling, which depends on a selected brain parcellation used for the calculation of the structural connectivity and derivation of the model network. Our findings provide suggestions for the optimal data processing for neuroimaging research and brain modeling.


2020 ◽  
Author(s):  
Anira Escrichs ◽  
Carles Biarnes ◽  
Josep Garre-Olmo ◽  
José Manuel Fernández-Real ◽  
Rafel Ramos ◽  
...  

Abstract Normal aging causes disruptions in the brain that can lead to cognitive decline. Resting-state functional magnetic resonance imaging studies have found significant age-related alterations in functional connectivity across various networks. Nevertheless, most of the studies have focused mainly on static functional connectivity. Studying the dynamics of resting-state brain activity across the whole-brain functional network can provide a better characterization of age-related changes. Here, we employed two data-driven whole-brain approaches based on the phase synchronization of blood-oxygen-level-dependent signals to analyze resting-state fMRI data from 620 subjects divided into two groups (middle-age group (n = 310); age range, 50–64 years versus older group (n = 310); age range, 65–91 years). Applying the intrinsic-ignition framework to assess the effect of spontaneous local activation events on local–global integration, we found that the older group showed higher intrinsic ignition across the whole-brain functional network, but lower metastability. Using Leading Eigenvector Dynamics Analysis, we found that the older group showed reduced ability to access a metastable substate that closely overlaps with the so-called rich club. These findings suggest that functional whole-brain dynamics are altered in aging, probably due to a deficiency in a metastable substate that is key for efficient global communication in the brain.


2020 ◽  
Vol 4 (3) ◽  
pp. 807-851
Author(s):  
Andreas Spiegler ◽  
Javad Karimi Abadchi ◽  
Majid Mohajerani ◽  
Viktor K. Jirsa

Resting-state functional networks such as the default mode network (DMN) dominate spontaneous brain dynamics. To date, the mechanisms linking brain structure and brain dynamics and functions in cognition, perception, and action remain unknown, mainly due to the uncontrolled and erratic nature of the resting state. Here we used a stimulation paradigm to probe the brain’s resting behavior, providing insights on state-space stability and multiplicity of network trajectories after stimulation. We performed explorations on a mouse model to map spatiotemporal brain dynamics as a function of the stimulation site. We demonstrated the emergence of known functional networks in brain responses. Several responses heavily relied on the DMN and were suggestive of the DMN playing a mechanistic role between functional networks. We probed the simulated brain responses to the stimulation of regions along the information processing chains of sensory systems from periphery up to primary sensory cortices. Moreover, we compared simulated dynamics against in vivo brain responses to optogenetic stimulation. Our results underwrite the importance of anatomical connectivity in the functional organization of brain networks and demonstrate how functionally differentiated information processing chains arise from the same system.


2019 ◽  
Vol 116 (52) ◽  
pp. 26961-26969 ◽  
Author(s):  
Francesca Melozzi ◽  
Eyal Bergmann ◽  
Julie A. Harris ◽  
Itamar Kahn ◽  
Viktor Jirsa ◽  
...  

Whole brain dynamics intuitively depend upon the internal wiring of the brain; but to which extent the individual structural connectome constrains the corresponding functional connectome is unknown, even though its importance is uncontested. After acquiring structural data from individual mice, we virtualized their brain networks and simulated in silico functional MRI data. Theoretical results were validated against empirical awake functional MRI data obtained from the same mice. We demonstrate that individual structural connectomes predict the functional organization of individual brains. Using a virtual mouse brain derived from the Allen Mouse Brain Connectivity Atlas, we further show that the dominant predictors of individual structure–function relations are the asymmetry and the weights of the structural links. Model predictions were validated experimentally using tracer injections, identifying which missing connections (not measurable with diffusion MRI) are important for whole brain dynamics in the mouse. Individual variations thus define a specific structural fingerprint with direct impact upon the functional organization of individual brains, a key feature for personalized medicine.


2018 ◽  
Author(s):  
Amit Naskar ◽  
Anirudh Vattikonda ◽  
Gustavo Deco ◽  
Dipanjan Roy ◽  
Arpan Banerjee

AbstractPrevious neuro-computational studies have established the connection of spontaneous resting-state brain activity with “large-scale” neuronal ensembles using dynamic mean field approach and showed the impact of local excitatory−inhibitory (E−I) balance in sculpting dynamical patterns. Here, we argue that whole brain models that link multiple scales of physiological organization namely brain metabolism that governs synaptic concentrations of gamma-aminobutyric acid (GABA) and glutamate on one hand and neural field dynamics that operate on the macroscopic scale. The multiscale dynamic mean field (MDMF) model captures the synaptic gating dynamics over a cortical macrocolumn as a function of neurotransmitter kinetics. Multiple MDMF units were placed in brain locations guided by an anatomical parcellation and connected by tractography data from diffusion tensor imaging. The resulting whole-brain model generates the resting-state functional connectivity and also reveal that optimal configurations of glutamate and GABA captures the dynamic working point of the brain, that is the state of maximum metsatability as observed in BOLD signals. To demonstrate test-retest reliability we validate the observation that healthy resting brain dynamics is governed by optimal glutamate-GABA configurations using two different brain parcellations for model set-up. Furthermore, graph theoretical measures of segregation (modularity and clustering coefficient) and integration (global efficiency and characteristic path length) on the functional connectivity generated from healthy and pathological brain network studies could be explained by the MDMF model. In conclusion, the MDMF model could relate the various scales of observations from neurotransmitter concentrations to dynamics of synaptic gating to whole-brain resting-state network topology in health and disease.


2020 ◽  
Author(s):  
Anira Escrichs ◽  
Carles Biarnes ◽  
Josep Garre-Olmo ◽  
José Manuel Fernández-Real ◽  
Rafel Ramos ◽  
...  

AbstractNormal aging causes disruptions in the brain that can lead to cognitive decline. Resting-state fMRI studies have found significant age-related alterations in functional connectivity across various networks. Nevertheless, most of the studies have focused mainly on static functional connectivity. Studying the dynamics of resting-state brain activity across the whole-brain functional network can provide a better characterization of age-related changes. Here we employed two data-driven whole-brain approaches based on the phase synchronization of blood-oxygen-level-dependent (BOLD) signals to analyze resting-state fMRI data from 620 subjects divided into two groups (‘middle-age group’ (n=310); age range, 50-65 years vs. ‘older group’ (n=310); age range, 66-91 years). Applying the Intrinsic-Ignition Framework to assess the effect of spontaneous local activation events on local-global integration, we found that the older group showed higher intrinsic ignition across the whole-brain functional network, but lower metastability. Using Leading Eigenvector Dynamics Analysis, we found that the older group showed reduced ability to access a metastable substate that closely overlaps with the so-called rich club. These findings suggest that functional whole-brain dynamics are altered in aging, probably due to a deficiency in a metastable substate that is key for efficient global communication in the brain.


2021 ◽  
Author(s):  
Robyn L. Miller ◽  
Victor M Vergara ◽  
Vince Calhoun

The most common pipelines for studying time-varying network connectivity in resting state functional magnetic resonance imaging (rs-fMRI) operate at the whole brain level, capturing a small discrete set of 'states' that best represent time-resolved joint measures of connectivity over all network pairs in the brain. This whole-brain hidden Markov model (HMM) approach 'uniformizes' the dynamics over what is typically more than 1000 pairs of networks, forcing each time-resolved high-dimensional observation into its best-matched high-dimensional state. While straightforward and convenient, this HMM simplification obscures functional and temporal nonstationarities that could reveal systematic, informative features of resting state brain dynamics at a more granular scale. We introduce a framework for studying functionally localized dynamics that intrinsically embeds them within a whole-brain HMM frame of reference. The approach is validated in a large rs-fMRI schizophrenia study where it identifies group differences in localized patterns of entropy and dynamics that help explain consistently observed differences between schizophrenia patients and controls in occupancy of whole-brain dFNC states more mechanistically.


Author(s):  
Patricio Donnelly‐Kehoe ◽  
Victor M. Saenger ◽  
Nina Lisofsky ◽  
Simone Kühn ◽  
Morten L. Kringelbach ◽  
...  

2019 ◽  
Vol 50 (11) ◽  
pp. 1852-1861 ◽  
Author(s):  
Du Lei ◽  
Walter H. L. Pinaya ◽  
Therese van Amelsvoort ◽  
Machteld Marcelis ◽  
Gary Donohoe ◽  
...  

AbstractBackgroundPrevious studies using resting-state functional neuroimaging have revealed alterations in whole-brain images, connectome-wide functional connectivity and graph-based metrics in groups of patients with schizophrenia relative to groups of healthy controls. However, it is unclear which of these measures best captures the neural correlates of this disorder at the level of the individual patient.MethodsHere we investigated the relative diagnostic value of these measures. A total of 295 patients with schizophrenia and 452 healthy controls were investigated using resting-state functional Magnetic Resonance Imaging at five research centres. Connectome-wide functional networks were constructed by thresholding correlation matrices of 90 brain regions, and their topological properties were analyzed using graph theory-based methods. Single-subject classification was performed using three machine learning (ML) approaches associated with varying degrees of complexity and abstraction, namely logistic regression, support vector machine and deep learning technology.ResultsConnectome-wide functional connectivity allowed single-subject classification of patients and controls with higher accuracy (average: 81%) than both whole-brain images (average: 53%) and graph-based metrics (average: 69%). Classification based on connectome-wide functional connectivity was driven by a distributed bilateral network including the thalamus and temporal regions.ConclusionThese results were replicated across the three employed ML approaches. Connectome-wide functional connectivity permits differentiation of patients with schizophrenia from healthy controls at single-subject level with greater accuracy; this pattern of results is consistent with the ‘dysconnectivity hypothesis’ of schizophrenia, which states that the neural basis of the disorder is best understood in terms of system-level functional connectivity alterations.


2020 ◽  
Author(s):  
Erfan Nozari ◽  
Jennifer Stiso ◽  
Lorenzo Caciagli ◽  
Eli J. Cornblath ◽  
Xiaosong He ◽  
...  

AbstractA central challenge in the computational modeling of neural dynamics is the trade-off between accuracy and simplicity. At the level of individual neurons, nonlinear dynamics are both experimentally established and essential for neuronal functioning. One may therefore expect the collective dynamics of massive networks of such neurons to only increase in their complexity, thereby supporting an expanded repertoire of nonlinear behaviors. An implicit assumption has thus formed that an “accurate” computational model of whole-brain dynamics must inevitably be nonlinear whereas linear models may provide a first-order approximation. To what extent this assumption holds, however, has remained an open question. Here, we provide a rigorous and data-driven answer at the level of whole-brain blood-oxygen-level-dependent (BOLD) and macroscopic field potential dynamics by leveraging the theory of system identification. Using functional magnetic resonance imaging (fMRI) and intracranial electroencephalography (iEEG), we model the spontaneous, resting state activity of 700 subjects in the Human Connectome Project (HCP) and 122 subjects from the Restoring Active Memory (RAM) project using state-of-the-art linear and nonlinear model families. We assess relative model fit using predictive power, computational complexity, and the extent of residual dynamics unexplained by the model. Contrary to our expectations, linear auto-regressive models achieve the best measures across all three metrics, eliminating the trade-off between accuracy and simplicity. To understand and explain this linearity, we highlight four properties of macroscopic neurodynamics which can counteract or mask microscopic nonlinear dynamics: averaging over space, averaging over time, observation noise, and limited data samples. Whereas the latter two are technological limitations and can improve in the future, the former two are inherent to aggregated macroscopic brain activity. Our results demonstrate the discounted potential of linear models in accurately capturing macroscopic brain dynamics. This, together with the unparalleled interpretability of linear models, can greatly facilitate our understanding of macroscopic neural dynamics, which in turn may facilitate the principled design of model-based interventions for the treatment of neuropsychiatric disorders.


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