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Structural determinants of dynamic fluctuations between segregation and integration on the human connectome.

ABSTRACT: While segregation and integration of neural information in the neocortex are thought to be important for human behavior and cognition, the neural substrates enabling their dynamic fluctuations remain elusive. To tackle this problem, we aim to identify specific network features of the connectome that are responsible for the emergence of dynamic fluctuations between segregated and integrated patterns in human resting-state functional connectivity. Here we examine the contributions of network features to dynamic fluctuations by constructing rewired surrogate connectome in which network features of interest are selectively preserved, and then by assessing the magnitude of fluctuations simulated with these surrogates. Our analysis demonstrates significant contributions from global geometry and topology of the connectome, as well as from localized structural connections involving visual areas. By providing structural accounts of dynamic fluctuations in functional connectivity, this study offers new insights into generative mechanisms driving temporal changes in segregation and integration in the brain.

SUBMITTER: Fukushima M

PROVIDER: S-EPMC7584581 | biostudies-literature | 2020 Oct

REPOSITORIES: biostudies-literature

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Structural determinants of dynamic fluctuations between segregation and integration on the human connectome.

Fukushima Makoto M Sporns Olaf O

Communications biology 20201023 1

While segregation and integration of neural information in the neocortex are thought to be important for human behavior and cognition, the neural substrates enabling their dynamic fluctuations remain elusive. To tackle this problem, we aim to identify specific network features of the connectome that are responsible for the emergence of dynamic fluctuations between segregated and integrated patterns in human resting-state functional connectivity. Here we examine the contributions of network featu ...[more]

PMID: 33097809

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Project description:The primate connectome, possessing a characteristic global topology and specific regional connectivity profiles, is well organized to support both segregated and integrated brain function. However, the organization mechanisms shaping the characteristic connectivity and its relationship to functional requirements remain unclear. The primate brain connectome is shaped by metabolic economy as well as functional values. Here, we explored the influence of two competing factors and additional advanced functional requirements on the primate connectome employing an optimal trade-off model between neural wiring cost and the representative functional requirement of processing efficiency. Moreover, we compared this model with a generative model combining spatial distance and topological similarity, with the objective of statistically reproducing multiple topological features of the network. The primate connectome indeed displays a cost-efficiency trade-off and that up to 67% of the connections were recovered by optimal combination of the two basic factors of wiring economy and processing efficiency, clearly higher than the proportion of connections (56%) explained by the generative model. While not explicitly aimed for, the trade-off model captured several key topological features of the real connectome as the generative model, yet better explained the connectivity of most regions. The majority of the remaining 33% of connections unexplained by the best trade-off model were long-distance links, which are concentrated on few cortical areas, termed long-distance connectors (LDCs). The LDCs are mainly non-hubs, but form a densely connected group overlapping on spatially segregated functional modalities. LDCs are crucial for both functional segregation and integration across different scales. These organization features revealed by the optimization analysis provide evidence that the demands of advanced functional segregation and integration among spatially distributed regions may play a significant role in shaping the cortical connectome, in addition to the basic cost-efficiency trade-off. These findings also shed light on inherent vulnerabilities of brain networks in diseases.

Project description:BackgroundPrevious studies on brain functional connectivity have revealed the neural physiopathology in patients with pontine stroke (PS). However, those studies focused only on the static features of intrinsic fluctuations, rather than on the time-varying effects throughout the entire scan. In the present study, we sought to explore the underlying mechanism of PS using the dynamic functional network connectivity (dFNC) method.MethodsResting-state functional magnetic resonance imaging (fMRI) data were collected from 58 patients with PS and 52 healthy controls (HC). Independent component analysis (ICA), the sliding window method, and k-means clustering analysis were performed to extract different functional networks, to calculate dFNC matrices, and to estimate distinct dynamic connectivity states. Additionally, temporal features were compared between the two groups in each state to explore the brain's preference for different dynamic connectivity states in PS, and global and local efficiency were compared among states to explore the differences of topologic organization across different dFNC states. The correlations between clinical scales and the temporal features that differed between the two groups also were calculated.ResultsThe dFNC analyses suggested four recurring states; in two of these states, the PS group showed a different duration from that of the HC group. Patients with PS spent significantly more time in a sparsely connected state (State 1), which was characterized by relatively low levels of connectivity within and between all brain networks. In contrast, patients with PS spent significantly less time in a highly segregated state (State 2), which was characterized by high levels of positive connectivities within primary perceptional domains and within higher cognitive control domains, and by high levels of negative inter-functional connectivities (inter-FCs) among primary perceptional and higher cognitive control domains. Additionally, the dwell time in State 2 was positively correlated with HC group's long-term memory scores in the Rey Auditory Verbal Learning Test (RAVLT-L), whereas there was no correlation between the State-2 dwell time and RAVLT-L scores in the PS group. Furthermore, the sparsely connected state and the highly segregated state mentioned above had the highest global efficiency and the highest local efficiency among the four states, respectively.ConclusionsIn summary, we observed a preference in the aberrant brain for dynamic connectivity states with different network topologic organization in patients with PS, indicating abnormal functional segregation and integration of the whole brain and confirming the imperfection of functional network connectivity in patients with PS. These findings provide new evidence for the dynamic neural mechanisms underlying clinical symptoms in patients with PS.

Dataset Information

Structural determinants of dynamic fluctuations between segregation and integration on the human connectome.

Publications

Structural determinants of dynamic fluctuations between segregation and integration on the human connectome.

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