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1.
Commun Biol ; 7(1): 126, 2024 01 24.
Article in English | MEDLINE | ID: mdl-38267534

ABSTRACT

Previous studies have adopted an edge-centric framework to study fine-scale network dynamics in human fMRI. To date, however, no studies have applied this framework to data collected from model organisms. Here, we analyze structural and functional imaging data from lightly anesthetized mice through an edge-centric lens. We find evidence of "bursty" dynamics and events - brief periods of high-amplitude network connectivity. Further, we show that on a per-frame basis events best explain static FC and can be divided into a series of hierarchically-related clusters. The co-fluctuation patterns associated with each cluster centroid link distinct anatomical areas and largely adhere to the boundaries of algorithmically detected functional brain systems. We then investigate the anatomical connectivity undergirding high-amplitude co-fluctuation patterns. We find that events induce modular bipartitions of the anatomical network of inter-areal axonal projections. Finally, we replicate these same findings in a human imaging dataset. In summary, this report recapitulates in a model organism many of the same phenomena observed in previously edge-centric analyses of human imaging data. However, unlike human subjects, the murine nervous system is amenable to invasive experimental perturbations. Thus, this study sets the stage for future investigation into the causal origins of fine-scale brain dynamics and high-amplitude co-fluctuations. Moreover, the cross-species consistency of the reported findings enhances the likelihood of future translation.


Subject(s)
Araceae , Connectome , Lens, Crystalline , Humans , Animals , Mice , Brain/diagnostic imaging , Axons
2.
Proc Natl Acad Sci U S A ; 120(30): e2300888120, 2023 07 25.
Article in English | MEDLINE | ID: mdl-37467265

ABSTRACT

The standard approach to modeling the human brain as a complex system is with a network, where the basic unit of interaction is a pairwise link between two brain regions. While powerful, this approach is limited by the inability to assess higher-order interactions involving three or more elements directly. In this work, we explore a method for capturing higher-order dependencies in multivariate data: the partial entropy decomposition (PED). Our approach decomposes the joint entropy of the whole system into a set of nonnegative atoms that describe the redundant, unique, and synergistic interactions that compose the system's structure. PED gives insight into the mathematics of functional connectivity and its limitation. When applied to resting-state fMRI data, we find robust evidence of higher-order synergies that are largely invisible to standard functional connectivity analyses. Our approach can also be localized in time, allowing a frame-by-frame analysis of how the distributions of redundancies and synergies change over the course of a recording. We find that different ensembles of regions can transiently change from being redundancy-dominated to synergy-dominated and that the temporal pattern is structured in time. These results provide strong evidence that there exists a large space of unexplored structures in human brain data that have been largely missed by a focus on bivariate network connectivity models. This synergistic structure is dynamic in time and likely will illuminate interesting links between brain and behavior. Beyond brain-specific application, the PED provides a very general approach for understanding higher-order structures in a variety of complex systems.


Subject(s)
Brain Mapping , Brain , Humans , Entropy , Brain/diagnostic imaging , Brain Mapping/methods , Magnetic Resonance Imaging/methods , Rest
3.
Neuroimage ; 277: 120266, 2023 08 15.
Article in English | MEDLINE | ID: mdl-37414231

ABSTRACT

Dynamic models of ongoing BOLD fMRI brain dynamics and models of communication strategies have been two important approaches to understanding how brain network structure constrains function. However, dynamic models have yet to widely incorporate one of the most important insights from communication models: the brain may not use all of its connections in the same way or at the same time. Here we present a variation of a phase delayed Kuramoto coupled oscillator model that dynamically limits communication between nodes on each time step. An active subgraph of the empirically derived anatomical brain network is chosen in accordance with the local dynamic state on every time step, thus coupling dynamics and network structure in a novel way. We analyze this model with respect to its fit to empirical time-averaged functional connectivity, finding that, with the addition of only one parameter, it significantly outperforms standard Kuramoto models with phase delays. We also perform analyses on the novel time series of active edges it produces, demonstrating a slowly evolving topology moving through intermittent episodes of integration and segregation. We hope to demonstrate that the exploration of novel modeling mechanisms and the investigation of dynamics of networks in addition to dynamics on networks may advance our understanding of the relationship between brain structure and function.


Subject(s)
Brain , Models, Neurological , Humans , Neural Pathways , Brain/diagnostic imaging , Brain Mapping/methods , Magnetic Resonance Imaging/methods , Nerve Net/diagnostic imaging
5.
Commun Biol ; 6(1): 451, 2023 04 24.
Article in English | MEDLINE | ID: mdl-37095282

ABSTRACT

One of the most well-established tools for modeling the brain is the functional connectivity network, which is constructed from pairs of interacting brain regions. While powerful, the network model is limited by the restriction that only pairwise dependencies are considered and potentially higher-order structures are missed. Here, we explore how multivariate information theory reveals higher-order dependencies in the human brain. We begin with a mathematical analysis of the O-information, showing analytically and numerically how it is related to previously established information theoretic measures of complexity. We then apply the O-information to brain data, showing that synergistic subsystems are widespread in the human brain. Highly synergistic subsystems typically sit between canonical functional networks, and may serve an integrative role. We then use simulated annealing to find maximally synergistic subsystems, finding that such systems typically comprise ≈10 brain regions, recruited from multiple canonical brain systems. Though ubiquitous, highly synergistic subsystems are invisible when considering pairwise functional connectivity, suggesting that higher-order dependencies form a kind of shadow structure that has been unrecognized by established network-based analyses. We assert that higher-order interactions in the brain represent an under-explored space that, accessible with tools of multivariate information theory, may offer novel scientific insights.


Subject(s)
Brain Mapping , Information Theory , Humans , Brain , Cerebral Cortex , Models, Neurological
6.
Neuroimage ; 250: 118971, 2022 04 15.
Article in English | MEDLINE | ID: mdl-35131435

ABSTRACT

Both cortical and subcortical regions can be functionally organized into networks. Regions of the basal ganglia are extensively interconnected with the cortex via reciprocal connections that relay and modulate cortical function. Here we employ an edge-centric approach, which computes co-fluctuations among region pairs in a network to investigate the role and interaction of subcortical regions with cortical systems. By clustering edges into communities, we show that cortical systems and subcortical regions couple via multiple edge communities, with hippocampus and amygdala having a distinct pattern from striatum and thalamus. We show that the edge community structure of cortical networks is highly similar to one obtained from cortical nodes when the subcortex is present in the network. Additionally, we show that the edge community profile of both cortical and subcortical nodes can be estimates solely from cortico-subcortical interactions. Finally, we used a motif analysis focusing on edge community triads where a subcortical region coupled to two cortical regions and found that two community triads where one community couples the subcortex to the cortex were overrepresented. In summary, our results show organized coupling of the subcortex to the cortex that may play a role in cortical organization of primary sensorimotor/attention and heteromodal systems and puts forth the motif analysis of edge community triads as a promising method for investigation of communication patterns in networks.


Subject(s)
Cerebral Cortex/diagnostic imaging , Connectome/methods , Magnetic Resonance Imaging/methods , Basal Ganglia/diagnostic imaging , Humans , Image Processing, Computer-Assisted , Nerve Net/diagnostic imaging , Neural Pathways/diagnostic imaging
7.
Proc Natl Acad Sci U S A ; 118(46)2021 11 16.
Article in English | MEDLINE | ID: mdl-34750261

ABSTRACT

The topology of structural brain networks shapes brain dynamics, including the correlation structure of brain activity (functional connectivity) as estimated from functional neuroimaging data. Empirical studies have shown that functional connectivity fluctuates over time, exhibiting patterns that vary in the spatial arrangement of correlations among segregated functional systems. Recently, an exact decomposition of functional connectivity into frame-wise contributions has revealed fine-scale dynamics that are punctuated by brief and intermittent episodes (events) of high-amplitude cofluctuations involving large sets of brain regions. Their origin is currently unclear. Here, we demonstrate that similar episodes readily appear in silico using computational simulations of whole-brain dynamics. As in empirical data, simulated events contribute disproportionately to long-time functional connectivity, involve recurrence of patterned cofluctuations, and can be clustered into distinct families. Importantly, comparison of event-related patterns of cofluctuations to underlying patterns of structural connectivity reveals that modular organization present in the coupling matrix shapes patterns of event-related cofluctuations. Our work suggests that brief, intermittent events in functional dynamics are partly shaped by modular organization of structural connectivity.


Subject(s)
Brain/physiology , Adult , Brain Mapping/methods , Computer Simulation , Female , Humans , Magnetic Resonance Imaging/methods , Male , Models, Neurological , Nerve Net/physiology , Neural Pathways/physiology , Young Adult
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