Dataset Information

Graph-theoretical analysis for energy landscape reveals the organization of state transitions in the resting-state human cerebral cortex.

ABSTRACT: The resting-state brain is often considered a nonlinear dynamic system transitioning among multiple coexisting stable states. Despite the increasing number of studies on the multistability of the brain system, the processes of state transitions have rarely been systematically explored. Thus, we investigated the state transition processes of the human cerebral cortex system at rest by introducing a graph-theoretical analysis of the state transition network. The energy landscape analysis of brain state occurrences, estimated using the pairwise maximum entropy model for resting-state fMRI data, identified multiple local minima, some of which mediate multi-step transitions toward the global minimum. The state transition among local minima is clustered into two groups according to state transition rates and most inter-group state transitions were mediated by a hub transition state. The distance to the hub transition state determined the path length of the inter-group transition. The cortical system appeared to have redundancy in inter-group transitions when the hub transition state was removed. Such a hub-like organization of transition processes disappeared when the connectivity of the cortical system was altered from the resting-state configuration. In the state transition, the default mode network acts as a transition hub, while coactivation of the prefrontal cortex and default mode network is captured as the global minimum. In summary, the resting-state cerebral cortex has a well-organized architecture of state transitions among stable states, when evaluated by a graph-theoretical analysis of the nonlinear state transition network of the brain.

SUBMITTER: Kang J

PROVIDER: S-EPMC6733463 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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Graph-theoretical analysis for energy landscape reveals the organization of state transitions in the resting-state human cerebral cortex.

Kang Jiyoung J Pae Chongwon C Park Hae-Jeong HJ

PloS one 20190909 9

The resting-state brain is often considered a nonlinear dynamic system transitioning among multiple coexisting stable states. Despite the increasing number of studies on the multistability of the brain system, the processes of state transitions have rarely been systematically explored. Thus, we investigated the state transition processes of the human cerebral cortex system at rest by introducing a graph-theoretical analysis of the state transition network. The energy landscape analysis of brain ...[more]

PMID: 31498822

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Project description:Background: Synchronous and antisynchronous activity between neural elements at rest reflects the physiological processes underlying complex cognitive ability. Regional and pairwise connectivity investigations suggest that perturbations in these activity patterns may relate to widespread cognitive impairments seen in bipolar disorder (BD). Here we take a network-based perspective to more meaningfully capture interactions among distributed brain regions compared to focal measurements and examine network-cognition relationships across a range of commonly affected cognitive domains in BD in relation to healthy controls. Methods: Resting-state networks were constructed as matrices of correlation coefficients between regionally averaged resting-state time series from 86 cortical/subcortical brain regions (FreeSurferv5.3.0). Cognitive performance measured using the Wechsler Adult Intelligence Scale, Cambridge Automated Neuropsychological Test Battery (CANTAB), and Reading the Mind in the Eyes tests was examined in relation to whole-brain connectivity measures and patterns of connectivity using a permutation-based statistical approach. Results: Faster response times in controls (n = 49) related to synchronous activity between frontal, parietal, cingulate, temporal, and occipital regions, while a similar response times in BD (n = 35) related to antisynchronous activity between regions of this subnetwork. Across all subjects, antisynchronous activity between the frontal, parietal, temporal, occipital, cingulate, insula, and amygdala regions related to improved memory performance. No resting-state subnetworks related to intelligence, executive function, short-term memory, or social cognition performance in the overall sample or in a manner that would explain deficits in these facets in BD. Conclusions: Our results demonstrate alterations in the intrinsic connectivity patterns underlying response timing in BD that are not specific to performance or errors on the same tasks. Across all individuals, no strong effects of resting-state global topology on cognition are found, while distinct functional networks supporting episodic and spatial memory highlight intrinsic inhibitory influences present in the resting state that facilitate memory processing. Impact Statement Regional and pairwise-connectivity investigations suggest altered interactions between brain areas may contribute to impairments in cognition that are observed in bipolar disorder. However, the distributed nature of these interactions across the brain remains poorly understood. Using recent advances in network neuroscience, we examine functional connectivity patterns associated with multiple cognitive domains in individuals with and without bipolar disorder. We discover distinct patterns of connectivity underlying response-timing performance uniquely in bipolar disorder and, independent of diagnosis, inhibitory interactions that relate to memory performance.

Project description:Interhemispheric connectivity with resting state MEG has been elusive, and demonstration of the default mode network (DMN) yet more challenging. Recent seed-based MEG analyses have shown interhemispheric connectivity using power envelope correlations. The purpose of this study is to compare graph theoretic maps of brain connectivity generated using MEG with and without signal leakage correction to evaluate for the presence of interhemispheric connectivity. Eight minutes of resting state eyes-open MEG data were obtained in 22 normal male subjects enrolled in an IRB-approved study (ages 16-18). Data were processed using an in-house automated MEG processing pipeline and projected into standard (MNI) source space at 7mm resolution using a scalar beamformer. Mean beta-band amplitude was sampled at 2.5second epochs from the source space time series. Leakage correction was performed in the time domain of the source space beam formed signal prior to amplitude transformation. Graph theoretic voxel-wise source space correlation connectivity analysis was performed for leakage corrected and uncorrected data. Degree maps were thresholded across subjects for the top 20% of connected nodes to identify hubs. Additional degree maps for sensory, visual, motor, and temporal regions were generated to identify interhemispheric connectivity using laterality indices. Hubs for the uncorrected MEG networks were predominantly symmetric and midline, bearing some resemblance to fMRI networks. These included the cingulate cortex, bilateral inferior frontal lobes, bilateral hippocampal formations and bilateral cerebellar hemispheres. These uncorrected networks however, demonstrated little to no interhemispheric connectivity using the ROI-based degree maps. Leakage corrected MEG data identified the DMN, with hubs in the posterior cingulate and biparietal areas. These corrected networks demonstrated robust interhemispheric connectivity for the ROI-based degree maps. Graph theoretic analysis of MEG resting state data without signal leakage correction can demonstrate symmetric networks with some resemblance to fMRI networks. These networks however, are an artifact of high local correlation from signal leakage and lack interhemispheric connectivity. Following signal leakage correction, MEG hubs emerge in the DMN, with strong interhemispheric connectivity.

Dataset Information

Graph-theoretical analysis for energy landscape reveals the organization of state transitions in the resting-state human cerebral cortex.

Publications

Graph-theoretical analysis for energy landscape reveals the organization of state transitions in the resting-state human cerebral cortex.

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