Explosive Synchronization-Based Brain Modulation Reduces Hypersensitivity in the Brain Network: A Computational Model Study

Kim, MinKyung; Harris, Richard E.; DaSilva, Alexandre F.; Lee, UnCheol

doi:10.3389/fncom.2022.815099

Cited by 10 publications

(9 citation statements)

References 71 publications

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“…Together, these results suggest an optimal intermediate ratio for a healthy brain as follows (Fig. 6d): Assume that the brain always operates at a resource bath size such that it is near the bistable region (criticality hypothesis 17,26 ). Moreover, the resource bath size also undergoes fluctuations.…”

Section: Resultsmentioning

confidence: 88%

“…These features are highly relevant to seizure dynamics, which also show signatures of critical transitions at both onset and termination across multiple spatial scales 15,16 . Consequently, ES models have been employed to study abrupt transitions in brain networks 17,18 . Moreover, complete brain coverage recordings, which can elucidate the dynamics of generalized seizures, are lacking in both patient and animal models.…”

Section: Introductionmentioning

confidence: 99%

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Interplay between resource dynamics, network structure and spatial propagation of transient explosive synchronization in an adaptively coupled mouse brain network model

Ranjan,

Gandhi

2023

Preprint

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Generalized epileptic attacks, which exhibit widespread disruption of brain activity, are characterized by recurrent, spontaneous and synchronized bursts of neural activity that self-initiate and self-terminate through critical transitions. Here we utilize the general framework of explosive synchronization (ES) from complex systems science to study the role of network structure and resource dynamics in the generation and propagation of seizures. We show that a combination of resource constraint and adaptive coupling in a Kuramoto network oscillator model can reliably generate seizure-like synchronization activity across different network topologies, including a biologically derived mesoscale mouse brain network. The model, coupled with a novel algorithm for tracking seizure propagation, provides mechanistic insight into the dynamics of transition to the synchronized state and its dependence on resources; and identifies key brain areas that may be involved in the initiation and spatial propagation of the seizure. The model, though minimal, efficiently recapitulates several experimental and theoretical predictions from more complex models, and makes novel experimentally testable predictions.Significance statement / Author SummaryUnderstanding seizure dynamics at the whole-brain level is crucial for controlling abnormal hypersynchronous activity. Currently, complete brain coverage recordings are lacking in both patients and animal models. We employ network science tools to investigate epileptic seizure-like synchronization in a mouse whole brain network, leveraging network structure and supported dynamics as the basis for seizure evolution. Our results align with experimental findings, suggesting that seizure activity initiates in the cortico-thalamic circuit. Importantly, our novel analysis identifies key nodes, primarily in the cortex, driving this hypersynchronous activity. Our findings highlight network structure’s role in shaping seizure dynamics and the techniques developed here could enhance our control of generalized seizures when combined with patient-specific data.

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Section: Resultsmentioning

confidence: 88%

Section: Introductionmentioning

confidence: 99%

Interplay between resource dynamics, network structure and spatial propagation of transient explosive synchronization in an adaptively coupled mouse brain network model

Ranjan,

Gandhi

2023

Preprint

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“…Stuart-Landau model is a mathematical model that describes the dynamics of coupled oscillator systems and their synchronization. The Stuart-Landau oscillator is extensively utilized for simulating the oscillatory dynamics between neural masses in the brain and for simulating brain signals from many different modalities [3,12,27]. In this study, we aim to investigate the sensitivity changes in the brain and the occurrence of crises using the Stuart-Landau model.…”

Section: Methodsmentioning

confidence: 99%

“…Discovering correlations between ES strength in the SCD brain, pain intensity, and frequency of VOCs could help us develop a novel treatment method to reduce pain intensity and frequency of pain crises. In a recent computational model, we showed that increasing connectivity in hub regions (e.g., insula, isthmus cingulate cortex, and precuneus) in an ES brain network can convert it into a non-ES brain network [27], which significantly reduces the brain's sensitivity to external stimuli. Our next step is to apply a stimulation method (e.g., acupuncture or transcranial direct current stimulation) that is known to alter brain connectivity [4,31] to our modeling approach.…”

Section: Es Can Provide a Theoretical Framework For The Treatment Of ...mentioning

confidence: 99%

Brain network hypersensitivity underlies pain crises in sickle cell disease

Joo,

Kim,

Kish

et al. 2023

Preprint

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Sickle cell disease (SCD) is a genetic disorder causing blood vessel blockages and painful Vaso-occlusive crises (VOCs). VOCs, characterized by severe pain due to blocked blood flow, are recurrent and unpredictable, posing challenges for preventive strategies. In this study we propose explosive synchronization (ES), a phenomenon characterized by abrupt brain network phase transitions, as a novel approach to address this challenge. We hypothesized that the accumulated disruptions in the brain network induced by SCD might lead to strengthened ES and hypersensitivity. We explored ES’s relationship with patient reported outcome measures (PROMs) and VOCs by analyzing EEG data from 25 SCD patients and 18 matched controls. SCD patients exhibited significantly lower alpha wave frequency than controls. SCD patients under painful pressure stimulation showed correlation between frequency disassortativity (FDA), an ES condition, and three important PROMs. Furthermore, patients who had a higher frequency of VOCs in the preceding 12 months presented with stronger FDA. The timing of VOC occurrence relative to EEG recordings was significantly associated to FDA. We also conducted computational modeling on SCD brain network to study FDA’s role in network sensitivity. Stronger FDA correlated with higher responsivity and complexity in our model. Simulation under noisy environment showed that higher FDA could be linked to increased occurrence frequency of crisis. This study establishes connections between SCD pain and the universal network mechanism, ES, offering a strong theoretical foundation. This understanding will aid predicting VOCs and refining pain management for SCD patients.

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“…Recent studies have suggested a link between ES in brain networks and chronic pain. We recently demonstrated that patients with fibromyalgia exhibit characteristics of ES on electroencephalography (EEG) that are associated with increased pain intensity 10 , and that modulation of brain networks can transform a sensitive network into an insensitive one, or one not prone to ES 11 . These modeling investigations provided valuable insights into the network-level mechanisms of fibromyalgia and provide a rationale for studying ES mechanisms in other pain populations such as SCD.…”

Section: Introductionmentioning

confidence: 99%

Brain network hypersensitivity underlies pain crises in sickle cell disease

Joo,

Kim,

Kish

et al. 2024

Sci Rep

Self Cite

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Sickle cell disease (SCD) is a genetic disorder causing painful and unpredictable Vaso-occlusive crises (VOCs) through blood vessel blockages. In this study, we propose explosive synchronization (ES) as a novel approach to comprehend the hypersensitivity and occurrence of VOCs in the SCD brain network. We hypothesized that the accumulated disruptions in the brain network induced by SCD might lead to strengthened ES and hypersensitivity. We explored ES's relationship with patient reported outcome measures (PROMs) as well as VOCs by analyzing EEG data from 25 SCD patients and 18 matched controls. SCD patients exhibited lower alpha frequency than controls. SCD patients showed correlation between frequency disassortativity (FDA), an ES condition, and three important PROMs. Furthermore, stronger FDA was observed in SCD patients with a higher frequency of VOCs and EEG recording near VOC. We also conducted computational modeling on SCD brain network to study FDA's role in network sensitivity. Our model demonstrated that a stronger FDA could be linked to increased sensitivity and frequency of VOCs. This study establishes connections between SCD pain and the universal network mechanism, ES, offering a strong theoretical foundation. This understanding will aid predicting VOCs and refining pain management for SCD patients.

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Explosive Synchronization-Based Brain Modulation Reduces Hypersensitivity in the Brain Network: A Computational Model Study

Cited by 10 publications

References 71 publications

Interplay between resource dynamics, network structure and spatial propagation of transient explosive synchronization in an adaptively coupled mouse brain network model

Interplay between resource dynamics, network structure and spatial propagation of transient explosive synchronization in an adaptively coupled mouse brain network model

Brain network hypersensitivity underlies pain crises in sickle cell disease

Brain network hypersensitivity underlies pain crises in sickle cell disease

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