Symbiotic relationship between brain structure and dynamics

Rubinov, Mikail; Sporns, Olaf; Leeuwen, Cees van; Breakspear, Michael

doi:10.1186/1471-2202-10-55

Cited by 187 publications

(181 citation statements)

References 63 publications

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“…These observations confirmed that the relationship between FCS and rCBF was not solely the result of structural covariates. A growing number of empirical (6,29) and computational (30,31) studies support the hypothesis that spontaneous neural activity is shaped, but not limited, by the underlying anatomy. Our observations suggest that metabolic demands also have a close relationship with intrinsic functional organization of the brain networks.…”

Section: Discussionmentioning

confidence: 94%

Coupling of functional connectivity and regional cerebral blood flow reveals a physiological basis for network hubs of the human brain

Liang

Zou

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

607

515

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Human brain functional networks contain a few densely connected hubs that play a vital role in transferring information across regions during resting and task states. However, the relationship of these functional hubs to measures of brain physiology, such as regional cerebral blood flow (rCBF), remains incompletely understood. Here, we used functional MRI data of blood-oxygenation-level-dependent and arterial-spin-labeling perfusion contrasts to investigate the relationship between functional connectivity strength (FCS) and rCBF during resting and an N-back working-memory task. During resting state, functional brain hubs with higher FCS were identified, primarily in the default-mode, insula, and visual regions. The FCS showed a striking spatial correlation with rCBF, and the correlation was stronger in the default-mode network (DMN; including medial frontal-parietal cortices) and executive control network (ECN; including lateral frontal-parietal cortices) compared with visual and sensorimotor networks. Moreover, the relationship was connection-distance dependent; i.e., rCBF correlated stronger with long-range hubs than short-range ones. It is notable that several DMN and ECN regions exhibited higher rCBF per unit connectivity strength (rCBF/FCS ratio); whereas, this index was lower in posterior visual areas. During the working-memory experiment, both FCS-rCBF coupling and rCBF/FCS ratio were modulated by task load in the ECN and/or DMN regions. Finally, task-induced changes of FCS and rCBF in the lateral-parietal lobe positively correlated with behavioral performance. Together, our results indicate a tight coupling between blood supply and brain functional topology during rest and its modulation in response to task demands, which may shed light on the physiological basis of human brain functional connectome.fMRI | connectomics | graph theory | modularity | metabolism T he human brain is a complex network that supports efficient communication through a collection of interconnected brain units, i.e., nodes (1, 2). Within the brain network, most nodes have few connections, but a few so-called hub nodes have a large number of connections (3-5). Graph-theory analysis of both human structural and functional connectivity data has revealed that these brain hubs are located predominantly in the posterior cingulate cortex/precuneus (PCC/PCu), medial-prefrontal cortex (mPFC), and lateral temporal and parietal cortices (4-8). Most of these brain regions constitute the putative default-mode network (DMN) that exhibits a high level of metabolism at rest (9). The spatial similarity between connectivity hubs and metabolism distribution suggests a relationship between intrinsic network connectivity and metabolic demands of the human brain.Brain metabolism includes oxidative phosphorylation, which consumes most of the glucose and produces most of the energy, and aerobic glycolysis, which accounts for a much smaller portion of the consumed glucose but is critical to a number of cellular functions (10). It has been shown that regio...

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Section: Discussionmentioning

confidence: 94%

Coupling of functional connectivity and regional cerebral blood flow reveals a physiological basis for network hubs of the human brain

Liang

Zou

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

607

515

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“…An alternative explanation is that these unusual pathways are the consequence of synesthetic experiences (Jancke et al 2009;Weiss and Fink 2009). Given that gray matter volume changes in the human adults' brain as a result of short periods of training have been demonstrated (Kwok et al 2011), and that brain dynamics are claimed to promote neuroanatomical self-organization (Rubinov et al 2009), the interpretation of synesthetic anatomical peculiarities as a result of repetitive intersensory coupling is not implausible. In this case, functional imbalance would be responsible for structural variations.…”

Section: The Canonical Regions Of Interestmentioning

confidence: 99%

Grapheme-color synesthetes show peculiarities in their emotional brain: cortical and subcortical evidence from VBM analysis of 3D-T1 and DTI data

et al. 2013

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Grapheme-color synesthesia is a neurological phenomenon in which viewing achromatic letters/numbers leads to automatic and involuntary color experiences. In this study, voxel-based morphometry analyses were performed on Tl images and fractional anisotropy measures to examine the whole brain in associator grapheme-color synesthetes. These analyses provide new evidence of variations in emotional areas (both at the cortical and subcortical levels), findings that help understand the emotional component as a relevant aspect of the synesthetic experience. Additionally, this study replicates previous findings in the left intraparietal sulcus and, for the first time, reports the existence of anatomical differences in subcortical gray nuclei of developmental grapheme-color synesthetes, providing a link between acquired and developmental synesthesia. This empirical evidence, which goes beyond modality-specific areas, could lead to a better understanding of grapheme-color synesthesia as well as of other modalities of the phenomenon.

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“…Theoretical work has related these dynamics to the generation of a "community architecture" of brain networks (12). Communities are groups of interacting brain regions that are more tightly functionally related to each other than to the rest of the brain.…”

mentioning

confidence: 99%

Dynamic brain network reconfiguration as a potential schizophrenia genetic risk mechanism modulated by NMDA receptor function

Braun

Schäfer

Bassett

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

190

184

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Schizophrenia is increasingly recognized as a disorder of distributed neural dynamics, but the molecular and genetic contributions are poorly understood. Recent work highlights a role for altered N-methyl-D-aspartate (NMDA) receptor signaling and related impairments in the excitation-inhibitory balance and synchrony of large-scale neural networks. Here, we combined a pharmacological intervention with novel techniques from dynamic network neuroscience applied to functional magnetic resonance imaging (fMRI) to identify alterations in the dynamic reconfiguration of brain networks related to schizophrenia genetic risk and NMDA receptor hypofunction. We quantified "network flexibility," a measure of the dynamic reconfiguration of the community structure of time-variant brain networks during working memory performance. Comparing 28 patients with schizophrenia, 37 unaffected first-degree relatives, and 139 healthy controls, we detected significant differences in network flexibility [F(2,196) = 6.541, P = 0.002] in a pattern consistent with the assumed genetic risk load of the groups (highest for patients, intermediate for relatives, and lowest for controls). In an observer-blinded, placebo-controlled, randomized, cross-over pharmacological challenge study in 37 healthy controls, we further detected a significant increase in network flexibility as a result of NMDA receptor antagonism with 120 mg dextromethorphan [F(1,34) = 5.291, P = 0.028]. Our results identify a potential dynamic network intermediate phenotype related to the genetic liability for schizophrenia that manifests as altered reconfiguration of brain networks during working memory. The phenotype appears to be influenced by NMDA receptor antagonism, consistent with a critical role for glutamate in the temporal coordination of neural networks and the pathophysiology of schizophrenia. S chizophrenia is a highly heritable mental disorder for which aberrant interactions between brain regions or "dysconnectivity" have been proposed as a core neural mechanism (1). Functional magnetic resonance imaging (fMRI) studies demonstrate alterations in specific neural subcircuits in schizophrenia (2, 3) that are under genetic control (4), although recent data from network neuroscience point to more widespread disturbances in the dynamics of large-scale brain networks (5, 6). Uhlhaas (5), Uhlhaas and Singer (6), and Phillips and Silverstein (7) have proposed a plausible pathophysiological mechanism for these phenomena: They argue that alterations in the cellular excitation-inhibitory balance may lead to disturbances in the neural synchrony of large-scale cell ensembles and give rise to the dysconnectivity phenomena at the level of neural ensembles.The neural excitation-inhibitory balance is highly dependent on glutamatergic N-methyl-D-aspartate (NMDA) receptor function (8), and alterations in NMDA receptor signaling have been associated with schizophrenia risk (9), disorder-related cognitive abnormalities (10, 11), and deficits in the temporal coordination of large-scale bra...

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Symbiotic relationship between brain structure and dynamics

Cited by 187 publications

References 63 publications

Coupling of functional connectivity and regional cerebral blood flow reveals a physiological basis for network hubs of the human brain

Coupling of functional connectivity and regional cerebral blood flow reveals a physiological basis for network hubs of the human brain

Grapheme-color synesthetes show peculiarities in their emotional brain: cortical and subcortical evidence from VBM analysis of 3D-T1 and DTI data

Dynamic brain network reconfiguration as a potential schizophrenia genetic risk mechanism modulated by NMDA receptor function

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