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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.


Modularity increased with hub connectivity suppressed. The ratio between the average intramodular synchrony of the functional modules and the whole brain synchrony is displayed for the cases in which either edges between hub nodes or random edges have been removed. Interestingly, when hub connectivity was suppressed, intramodular synchrony relative to global synchrony increased during the critical regime. Conversely, this increase in modularity was not observed when only random edges were removed
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Fig4: Modularity increased with hub connectivity suppressed. The ratio between the average intramodular synchrony of the functional modules and the whole brain synchrony is displayed for the cases in which either edges between hub nodes or random edges have been removed. Interestingly, when hub connectivity was suppressed, intramodular synchrony relative to global synchrony increased during the critical regime. Conversely, this increase in modularity was not observed when only random edges were removed

Mentions: Next, we examined the role of hub nodes in establishing global synchrony. Targeted suppression of structural connectivity was inflicted by computationally removing edges between hub nodes. For comparison, in a separate simulation, an equal number of random edges were removed. In simulations with suppressed connectivity (either between hubs or between random nodes), stronger cortical coupling was required for synchronization to compensate for the loss of connectivity, while the general shape of global synchronization progression towards a state of global synchrony remained the same (Additional file 4: Figure S4). However, simulations in which hub-to-hub connectivity was suppressed showed a significantly higher intramodular to global synchrony ratio than randomly suppressed connectivity simulations (Fig. 4) (p < 4.1 × l0−3, 104 random permutations of hub-to-hub and random connectivity suppressions, 0.015 < λ < 0.04). This increased intramodular to global synchrony ratio as seen in the hub suppressed network indicates that connections spanning between hub nodes (so-called ‘rich club connections’ [29]) play an important role in the integration of modules needed to reach global synchrony. Also in comparison with the unsuppressed, normal condition, suppression of hubs resulted in increased modularity (Additional file 5: Figure S5), again illustrating that without interconnected hub nodes, functional modules become more separated and the emergence of global synchrony is hampered.Fig. 4


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)

Modularity increased with hub connectivity suppressed. The ratio between the average intramodular synchrony of the functional modules and the whole brain synchrony is displayed for the cases in which either edges between hub nodes or random edges have been removed. Interestingly, when hub connectivity was suppressed, intramodular synchrony relative to global synchrony increased during the critical regime. Conversely, this increase in modularity was not observed when only random edges were removed
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

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

Fig4: Modularity increased with hub connectivity suppressed. The ratio between the average intramodular synchrony of the functional modules and the whole brain synchrony is displayed for the cases in which either edges between hub nodes or random edges have been removed. Interestingly, when hub connectivity was suppressed, intramodular synchrony relative to global synchrony increased during the critical regime. Conversely, this increase in modularity was not observed when only random edges were removed
Mentions: Next, we examined the role of hub nodes in establishing global synchrony. Targeted suppression of structural connectivity was inflicted by computationally removing edges between hub nodes. For comparison, in a separate simulation, an equal number of random edges were removed. In simulations with suppressed connectivity (either between hubs or between random nodes), stronger cortical coupling was required for synchronization to compensate for the loss of connectivity, while the general shape of global synchronization progression towards a state of global synchrony remained the same (Additional file 4: Figure S4). However, simulations in which hub-to-hub connectivity was suppressed showed a significantly higher intramodular to global synchrony ratio than randomly suppressed connectivity simulations (Fig. 4) (p < 4.1 × l0−3, 104 random permutations of hub-to-hub and random connectivity suppressions, 0.015 < λ < 0.04). This increased intramodular to global synchrony ratio as seen in the hub suppressed network indicates that connections spanning between hub nodes (so-called ‘rich club connections’ [29]) play an important role in the integration of modules needed to reach global synchrony. Also in comparison with the unsuppressed, normal condition, suppression of hubs resulted in increased modularity (Additional file 5: Figure S5), again illustrating that without interconnected hub nodes, functional modules become more separated and the emergence of global synchrony is hampered.Fig. 4

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.