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Mesoscopic physiological interactions in the human brain reveal small-world properties.

ABSTRACT: Cognition depends on rapid and robust communication between neural circuits spanning different brain areas. We investigated the mesoscopic network of cortico-cortical interactions in the human brain in an extensive dataset consisting of 6,024 h of intracranial field potential recordings from 4,142 electrodes in 48 subjects. We evaluated communication between brain areas at the network level across different frequency bands. The interaction networks were validated against known anatomical measurements and neurophysiological interactions in humans and monkeys. The resulting human brain interactome is characterized by a broad and spatially specific, dynamic, and extensive network. The physiological interactome reveals small-world properties, which we conjecture might facilitate efficient and reliable information transmission. The interaction dynamics correlate with the brain sleep/awake state. These results constitute initial steps toward understanding how the interactome orchestrates cortical communication and provide a reference for future efforts assessing how dysfunctional interactions may lead to mental disorders.

SUBMITTER: Wang J

PROVIDER: S-EPMC8457376 | biostudies-literature | 2021 Aug

REPOSITORIES: biostudies-literature

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Mesoscopic physiological interactions in the human brain reveal small-world properties.

Wang Jiarui J Tao Annabelle A Anderson William S WS Madsen Joseph R JR Kreiman Gabriel G

Cell reports 20210801 8

Cognition depends on rapid and robust communication between neural circuits spanning different brain areas. We investigated the mesoscopic network of cortico-cortical interactions in the human brain in an extensive dataset consisting of 6,024 h of intracranial field potential recordings from 4,142 electrodes in 48 subjects. We evaluated communication between brain areas at the network level across different frequency bands. The interaction networks were validated against known anatomical measure ...[more]

PMID: 34433053

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Project description:Evidence from imaging studies suggests that the human brain has a small-world network topology that might be disrupted in certain brain disorders. However, current methodology is based on global graph theory measures, such as clustering, C, characteristic path length, L, and small-worldness, S, that lack spatial specificity and are insufficient to identify regional brain abnormalities. Here we propose novel ultra-fast methodology for mapping local properties of brain network topology such as local C, L and S (lC, lL and lS) in the human brain at 3-mm isotropic resolution from 'resting-state' magnetic resonance imaging data. Test-retest datasets from 40 healthy children/adolescents were used to demonstrate the overall good reliability of the measures across sessions and computational parameters (intraclass correlation > 0.5 for lC and lL) and their low variability across subjects (< 29%). Whereas regions with high local functional connectivity density (lFCD; local degree) in posterior parietal and occipital cortices demonstrated high lC and short lL, subcortical regions (globus pallidus, thalamus, hippocampus and amygdala), cerebellum (lobes and vermis), cingulum and temporal cortex also had high, lS, demonstrating stronger small-world topology than other hubs. Children/adolescents had stronger lFCD, higher lC and longer lL in most cortical regions and thalamus than 74 healthy adults, consistent with pruning of functional connectivity during maturation. In contrast, lFCD, lC and lL were weaker in thalamus and midbrain, and lL was shorter in frontal cortical regions and cerebellum for 69 schizophrenia patients than for 74 healthy controls, suggesting exaggerated pruning of connectivity in schizophrenia. Follow up correlation analyses for seeds in thalamus and midbrain uncovered lower positive connectivity of these regions in thalamus, putamen, cerebellum and frontal cortex (cingulum, orbitofrontal, inferior frontal) and lower negative connectivity in auditory, visual, motor, premotor and somatosensory cortices for schizophrenia patients than for controls, consistent with prior findings of thalamic disconnection in schizophrenia.

Project description:Recently, increasing attention has been focused on the investigation of the human brain connectome that describes the patterns of structural and functional connectivity networks of the human brain. Many studies of the human connectome have demonstrated that the brain network follows a small-world topology with an intrinsically cohesive modular structure and includes several network hubs in the medial parietal regions. However, most of these studies have only focused on undirected connections between regions in which the directions of information flow are not taken into account. How the brain regions causally influence each other and how the directed network of human brain is topologically organized remain largely unknown. Here, we applied linear multivariate Granger causality analysis (GCA) and graph theoretical approaches to a resting-state functional MRI dataset with a large cohort of young healthy participants (n = 86) to explore connectivity patterns of the population-based whole-brain functional directed network. This directed brain network exhibited prominent small-world properties, which obviously improved previous results of functional MRI studies showing weak small-world properties in the directed brain networks in terms of a kernel-based GCA and individual analysis. This brain network also showed significant modular structures associated with 5 well known subsystems: fronto-parietal, visual, paralimbic/limbic, subcortical and primary systems. Importantly, we identified several driving hubs predominantly located in the components of the attentional network (e.g., the inferior frontal gyrus, supplementary motor area, insula and fusiform gyrus) and several driven hubs predominantly located in the components of the default mode network (e.g., the precuneus, posterior cingulate gyrus, medial prefrontal cortex and inferior parietal lobule). Further split-half analyses indicated that our results were highly reproducible between two independent subgroups. The current study demonstrated the directions of spontaneous information flow and causal influences in the directed brain networks, thus providing new insights into our understanding of human brain functional connectome.

Dataset Information

Mesoscopic physiological interactions in the human brain reveal small-world properties.

Publications

Mesoscopic physiological interactions in the human brain reveal small-world properties.

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