Dataset Information

Organization of Propagated Intrinsic Brain Activity in Individual Humans.

ABSTRACT: Spontaneous infra-slow (<0.1 Hz) fluctuations in functional magnetic resonance imaging (fMRI) signals are temporally correlated within large-scale functional brain networks, motivating their use for mapping systems-level brain organization. However, recent electrophysiological and hemodynamic evidence suggest state-dependent propagation of infra-slow fluctuations, implying a functional role for ongoing infra-slow activity. Crucially, the study of infra-slow temporal lag structure has thus far been limited to large groups, as analyzing propagation delays requires extensive data averaging to overcome sampling variability. Here, we use resting-state fMRI data from 11 extensively-sampled individuals to characterize lag structure at the individual level. In addition to stable individual-specific features, we find spatiotemporal topographies in each subject similar to the group average. Notably, we find a set of early regions that are common to all individuals, are preferentially positioned proximal to multiple functional networks, and overlap with brain regions known to respond to diverse behavioral tasks-altogether consistent with a hypothesized ability to broadly influence cortical excitability. Our findings suggest that, like correlation structure, temporal lag structure is a fundamental organizational property of resting-state infra-slow activity.

SUBMITTER: Raut RV

PROVIDER: S-EPMC7132930 | biostudies-literature | 2020 Mar

REPOSITORIES: biostudies-literature

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Organization of Propagated Intrinsic Brain Activity in Individual Humans.

Raut Ryan V RV Mitra Anish A Marek Scott S Ortega Mario M Snyder Abraham Z AZ Tanenbaum Aaron A Laumann Timothy O TO Dosenbach Nico U F NUF Raichle Marcus E ME

Cerebral cortex (New York, N.Y. : 1991) 20200301 3

Spontaneous infra-slow (<0.1 Hz) fluctuations in functional magnetic resonance imaging (fMRI) signals are temporally correlated within large-scale functional brain networks, motivating their use for mapping systems-level brain organization. However, recent electrophysiological and hemodynamic evidence suggest state-dependent propagation of infra-slow fluctuations, implying a functional role for ongoing infra-slow activity. Crucially, the study of infra-slow temporal lag structure has thus far be ...[more]

PMID: 31504262

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Project description:The characterization of topological architecture of complex brain networks is one of the most challenging issues in neuroscience. Slow (<0.1 Hz), spontaneous fluctuations of the blood oxygen level dependent (BOLD) signal in functional magnetic resonance imaging are thought to be potentially important for the reflection of spontaneous neuronal activity. Many studies have shown that these fluctuations are highly coherent within anatomically or functionally linked areas of the brain. However, the underlying topological mechanisms responsible for these coherent intrinsic or spontaneous fluctuations are still poorly understood. Here, we apply modern network analysis techniques to investigate how spontaneous neuronal activities in the human brain derived from the resting-state BOLD signals are topologically organized at both the temporal and spatial scales. We first show that the spontaneous brain functional networks have an intrinsically cohesive modular structure in which the connections between regions are much denser within modules than between them. These identified modules are found to be closely associated with several well known functionally interconnected subsystems such as the somatosensory/motor, auditory, attention, visual, subcortical, and the "default" system. Specifically, we demonstrate that the module-specific topological features can not be captured by means of computing the corresponding global network parameters, suggesting a unique organization within each module. Finally, we identify several pivotal network connectors and paths (predominantly associated with the association and limbic/paralimbic cortex regions) that are vital for the global coordination of information flow over the whole network, and we find that their lesions (deletions) critically affect the stability and robustness of the brain functional system. Together, our results demonstrate the highly organized modular architecture and associated topological properties in the temporal and spatial brain functional networks of the human brain that underlie spontaneous neuronal dynamics, which provides important implications for our understanding of how intrinsically coherent spontaneous brain activity has evolved into an optimal neuronal architecture to support global computation and information integration in the absence of specific stimuli or behaviors.

Project description:Emerging neuroimaging studies emphasize the dynamic organization of spontaneous brain activity in both human and non-human primates, even under anesthesia. In a recent study, we were able to characterize the heterogeneous architecture of intrinsic functional flexibility in the awake, resting human brain using time-resolved analysis and a probabilistic model. However, it is unknown whether this organizational principle is preserved in the anesthetized monkey brain, and how anesthesia affects dynamic and static measurements of spontaneous brain activity. To investigate these issues, we collected resting-state functional magnetic resonance imaging (fMRI) datasets from 178 awake humans and 11 anesthetized monkeys (all healthy). Our recently established method, a complexity measurement (i.e., Shannon entropy) of dynamic functional connectivity patterns of each brain region, was used to map the intrinsic functional flexibility across the cerebral cortex. To further explore the potential effects of anesthesia, we performed time series analysis and correlation analysis between dynamic and static measurements within awake human and anesthetized monkey brains, respectively. We observed a heterogeneous profile of intrinsic functional flexibility in the anesthetized monkey brain, which showed some similarities to that of awake humans (r = 0.30, p = 0.007). However, we found that brain activity in anesthetized monkeys generally shifted toward random fluctuations. Moreover, there is a negative correlation between nodal entropy for the distribution of dynamic functional connectivity patterns and static functional connectivity strength in anesthetized monkeys, but not in awake humans. Our findings indicate that the heterogeneous architecture of intrinsic functional flexibility across cortex probably reflects an evolutionarily conserved aspect of functional brain organization, which persists across levels of cognitive processing (states of consciousness). The coupling between nodal entropy for the distribution of dynamic functional connectivity patterns and static functional connectivity strength may serve as a potential signature of anesthesia. This study not only offers fresh insight into the evolution of brain functional architecture, but also advances our understanding of the dynamics of spontaneous brain activity.

Dataset Information

Organization of Propagated Intrinsic Brain Activity in Individual Humans.

Publications

Organization of Propagated Intrinsic Brain Activity in Individual Humans.

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