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Kuramoto model simulation of neural hubs and dynamic synchrony in the human cerebral connectome.

Schmidt R, LaFleur KJ, de Reus MA, van den Berg LH, van den Heuvel MP - BMC Neurosci (2015)

Bottom Line: Furthermore, suppressing structural connectivity among hub nodes resulted in an elevated modular state (p < 4.1 × l0(-3), 0.015 < λ < 0.04), indicating that hub-to-hub connections are critical in intermodular synchronization.Finally, perturbing the oscillatory behavior of hub nodes prevented functional modules from synchronizing, implying that synchronization of functional modules is dependent on the hub nodes' behavior.Our results converge on anatomical hubs having a leading role in intermodular synchronization and integration in the human brain.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurology, Brain Center Rudolf Magnus, University Medical Center Utrecht, Heidelberglaan 100, PO Box 85500, 3508 GA, Utrecht, Netherlands. r.schmidt@umcutrecht.nl.

ABSTRACT

Background: The topological structure of the wiring of the mammalian brain cortex plays an important role in shaping the functional dynamics of large-scale neural activity. Due to their central embedding in the network, high degree hub regions and their connections (often referred to as the 'rich club') have been hypothesized to facilitate intermodular neural communication and global integration of information by means of synchronization. Here, we examined the theoretical role of anatomical hubs and their wiring in brain dynamics. The Kuramoto model was used to simulate interaction of cortical brain areas by means of coupled phase oscillators-with anatomical connections between regions derived from diffusion weighted imaging and module assignment of brain regions based on empirically determined resting-state data.

Results: Our findings show that synchrony among hub nodes was higher than any module's intramodular synchrony (p < 10(-4), for cortical coupling strengths, λ, in the range 0.02 < λ < 0.05), suggesting that hub nodes lead the functional modules in the process of synchronization. Furthermore, suppressing structural connectivity among hub nodes resulted in an elevated modular state (p < 4.1 × l0(-3), 0.015 < λ < 0.04), indicating that hub-to-hub connections are critical in intermodular synchronization. Finally, perturbing the oscillatory behavior of hub nodes prevented functional modules from synchronizing, implying that synchronization of functional modules is dependent on the hub nodes' behavior.

Conclusion: Our results converge on anatomical hubs having a leading role in intermodular synchronization and integration in the human brain.

No MeSH data available.


Related in: MedlinePlus

Intramodular synchrony progression. Panela shows the evolution of intramodular synchrony within each of the 11 functional modules. The aberration of the Frontal module near whole brain synchrony is due to a single low-degree node. Panelb compares the intramodular synchrony of the modules to that of the hub nodes. Notably, the hub nodes led all of the functional modules in intramodular synchrony even though they were spatially distributed across the functional modules, and possessed a structural density on par with the average of the functional modules. Panelc shows the influence of each of the 11 modules and the hub nodes on the frequency of Default Mode Network nodes. The hub nodes become dominant in the process of global synchronization during the critical regime
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Fig3: Intramodular synchrony progression. Panela shows the evolution of intramodular synchrony within each of the 11 functional modules. The aberration of the Frontal module near whole brain synchrony is due to a single low-degree node. Panelb compares the intramodular synchrony of the modules to that of the hub nodes. Notably, the hub nodes led all of the functional modules in intramodular synchrony even though they were spatially distributed across the functional modules, and possessed a structural density on par with the average of the functional modules. Panelc shows the influence of each of the 11 modules and the hub nodes on the frequency of Default Mode Network nodes. The hub nodes become dominant in the process of global synchronization during the critical regime

Mentions: Intramodular synchrony, reflecting the share of in-phase nodes within a functional module, was observed to evolve as an s-curve with respect to coupling strength in all 11 functional modules (Fig. 3a) again with a critical regime between λ = 0.02 and λ = 0.04 showing a steep increase in intramodular synchrony similar to global synchrony (Fig. 2). In Fig. 3b the synchronization among the hub nodes (intra-hub synchrony) is contrasted with the intramodular synchrony levels observed in each of the 11 functional modules. While similar in shape, the curve corresponding to the hub nodes is observed to be shifted towards lower cortical coupling strengths with respect to the graphs of the functional modules. In other words, intra-hub synchrony is higher than any module’s intramodular synchrony (p < 10−4, 104 random permutations of connection labels ‘intra-hub’ and ‘intramodular’, 0.02 < λ < 0.05), implying that the rich club structure, spread out across the brain network and involved in all functional modules, requires less cortical coupling in order to reach synchrony than the similarly dense or even denser functional modules.Fig. 3


Kuramoto model simulation of neural hubs and dynamic synchrony in the human cerebral connectome.

Schmidt R, LaFleur KJ, de Reus MA, van den Berg LH, van den Heuvel MP - BMC Neurosci (2015)

Intramodular synchrony progression. Panela shows the evolution of intramodular synchrony within each of the 11 functional modules. The aberration of the Frontal module near whole brain synchrony is due to a single low-degree node. Panelb compares the intramodular synchrony of the modules to that of the hub nodes. Notably, the hub nodes led all of the functional modules in intramodular synchrony even though they were spatially distributed across the functional modules, and possessed a structural density on par with the average of the functional modules. Panelc shows the influence of each of the 11 modules and the hub nodes on the frequency of Default Mode Network nodes. The hub nodes become dominant in the process of global synchronization during the critical regime
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4556019&req=5

Fig3: Intramodular synchrony progression. Panela shows the evolution of intramodular synchrony within each of the 11 functional modules. The aberration of the Frontal module near whole brain synchrony is due to a single low-degree node. Panelb compares the intramodular synchrony of the modules to that of the hub nodes. Notably, the hub nodes led all of the functional modules in intramodular synchrony even though they were spatially distributed across the functional modules, and possessed a structural density on par with the average of the functional modules. Panelc shows the influence of each of the 11 modules and the hub nodes on the frequency of Default Mode Network nodes. The hub nodes become dominant in the process of global synchronization during the critical regime
Mentions: Intramodular synchrony, reflecting the share of in-phase nodes within a functional module, was observed to evolve as an s-curve with respect to coupling strength in all 11 functional modules (Fig. 3a) again with a critical regime between λ = 0.02 and λ = 0.04 showing a steep increase in intramodular synchrony similar to global synchrony (Fig. 2). In Fig. 3b the synchronization among the hub nodes (intra-hub synchrony) is contrasted with the intramodular synchrony levels observed in each of the 11 functional modules. While similar in shape, the curve corresponding to the hub nodes is observed to be shifted towards lower cortical coupling strengths with respect to the graphs of the functional modules. In other words, intra-hub synchrony is higher than any module’s intramodular synchrony (p < 10−4, 104 random permutations of connection labels ‘intra-hub’ and ‘intramodular’, 0.02 < λ < 0.05), implying that the rich club structure, spread out across the brain network and involved in all functional modules, requires less cortical coupling in order to reach synchrony than the similarly dense or even denser functional modules.Fig. 3

Bottom Line: Furthermore, suppressing structural connectivity among hub nodes resulted in an elevated modular state (p < 4.1 × l0(-3), 0.015 < λ < 0.04), indicating that hub-to-hub connections are critical in intermodular synchronization.Finally, perturbing the oscillatory behavior of hub nodes prevented functional modules from synchronizing, implying that synchronization of functional modules is dependent on the hub nodes' behavior.Our results converge on anatomical hubs having a leading role in intermodular synchronization and integration in the human brain.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurology, Brain Center Rudolf Magnus, University Medical Center Utrecht, Heidelberglaan 100, PO Box 85500, 3508 GA, Utrecht, Netherlands. r.schmidt@umcutrecht.nl.

ABSTRACT

Background: The topological structure of the wiring of the mammalian brain cortex plays an important role in shaping the functional dynamics of large-scale neural activity. Due to their central embedding in the network, high degree hub regions and their connections (often referred to as the 'rich club') have been hypothesized to facilitate intermodular neural communication and global integration of information by means of synchronization. Here, we examined the theoretical role of anatomical hubs and their wiring in brain dynamics. The Kuramoto model was used to simulate interaction of cortical brain areas by means of coupled phase oscillators-with anatomical connections between regions derived from diffusion weighted imaging and module assignment of brain regions based on empirically determined resting-state data.

Results: Our findings show that synchrony among hub nodes was higher than any module's intramodular synchrony (p < 10(-4), for cortical coupling strengths, λ, in the range 0.02 < λ < 0.05), suggesting that hub nodes lead the functional modules in the process of synchronization. Furthermore, suppressing structural connectivity among hub nodes resulted in an elevated modular state (p < 4.1 × l0(-3), 0.015 < λ < 0.04), indicating that hub-to-hub connections are critical in intermodular synchronization. Finally, perturbing the oscillatory behavior of hub nodes prevented functional modules from synchronizing, implying that synchronization of functional modules is dependent on the hub nodes' behavior.

Conclusion: Our results converge on anatomical hubs having a leading role in intermodular synchronization and integration in the human brain.

No MeSH data available.


Related in: MedlinePlus