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High-order information analysis of epileptogenesis in the pilocarpine rat model of temporal lobe epilepsy

(2025) ENEURO. 12(5).
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Abstract
Temporal lobe epilepsy (TLE) is a devastating disease, often pharmacoresistant and with a high prevalence of 1% worldwide. There are few disease-modifying therapies; thus, prevention has become a health priority. The overarching goal of this research project is to highlight the system's dynamics at different stages before TLE onset to identify an early shift in network dynamics trajectory towards disease onset. Researchers often investigate collective brain activity by tracking dynamical interactions of the signal recorded at multiple sites. However, these interactions are usually only computed between pairs of brain regions, at the risk of missing simultaneous interactions of three or more areas, an aspect that is crucial in a networked disease such as TLE. We thus propose to track, on a rich dataset of electrophysiological brain signals recorded within the TL of adult male Wistar Han rats, the formation and dissolution of high-order informational multiplets in time during distinct natural behaviors in an animal model of TLE. We identified the informational content of the multiplets as synergistic or redundant. Results identified an early transition of synergistic and redundant multiplets ahead of TLE onset with the predominant involvement of four TL brain regions in generating theta (4-12 Hz) activity. This shift has been shown predominantly during exploration, a theta-dependent behavior, less during rest and sleep. This specific change suggests a shift in communication from an integrated to a segregated network toward TLE onset.</jats:p><jats:p><jats:bold>Significance Statement</jats:bold>Temporal lobe epilepsy (TLE) is a prevalent network disorder that is often pharmacoresistant; therefore, TLE prevention is critical. This research article identifies early signs of TLE by studying collective dynamics within the TL using an information decomposition technique during natural behaviors. This computational method, beyond pairwise interactions, may thus need to be used to identify early biomarkers for TLE onset.
Keywords
epilepsy, information theory, computational neuroscience, signal processing, complex systems, animal study, electrophysiology in vivo, epileptogenesis, higher-order interactions, prediction, temporal lobe epilepsy, BRAIN INSULTS, THETA RHYTHM, INTEGRATION, SEQUENCES, ONSET

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Citation

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MLA
Mirjebreili, Morteza, et al. “High-Order Information Analysis of Epileptogenesis in the Pilocarpine Rat Model of Temporal Lobe Epilepsy.” ENEURO, vol. 12, no. 5, 2025, doi:10.1523/eneuro.0403-24.2025.
APA
Mirjebreili, M., Martinez de Aguirre Ibarreta, J., Marinazzo, D., & Chauvière, L. (2025). High-order information analysis of epileptogenesis in the pilocarpine rat model of temporal lobe epilepsy. ENEURO, 12(5). https://doi.org/10.1523/eneuro.0403-24.2025
Chicago author-date
Mirjebreili, Morteza, Josu Martinez de Aguirre Ibarreta, Daniele Marinazzo, and Laetitia Chauvière. 2025. “High-Order Information Analysis of Epileptogenesis in the Pilocarpine Rat Model of Temporal Lobe Epilepsy.” ENEURO 12 (5). https://doi.org/10.1523/eneuro.0403-24.2025.
Chicago author-date (all authors)
Mirjebreili, Morteza, Josu Martinez de Aguirre Ibarreta, Daniele Marinazzo, and Laetitia Chauvière. 2025. “High-Order Information Analysis of Epileptogenesis in the Pilocarpine Rat Model of Temporal Lobe Epilepsy.” ENEURO 12 (5). doi:10.1523/eneuro.0403-24.2025.
Vancouver
1.
Mirjebreili M, Martinez de Aguirre Ibarreta J, Marinazzo D, Chauvière L. High-order information analysis of epileptogenesis in the pilocarpine rat model of temporal lobe epilepsy. ENEURO. 2025;12(5).
IEEE
[1]
M. Mirjebreili, J. Martinez de Aguirre Ibarreta, D. Marinazzo, and L. Chauvière, “High-order information analysis of epileptogenesis in the pilocarpine rat model of temporal lobe epilepsy,” ENEURO, vol. 12, no. 5, 2025.
@article{01JSKZ1Q2D12F24FN117X19SEH,
  abstract     = {{Temporal lobe epilepsy (TLE) is a devastating disease, often pharmacoresistant and with a high prevalence of 1% worldwide. There are few disease-modifying therapies; thus, prevention has become a health priority. The overarching goal of this research project is to highlight the system's dynamics at different stages before TLE onset to identify an early shift in network dynamics trajectory towards disease onset. Researchers often investigate collective brain activity by tracking dynamical interactions of the signal recorded at multiple sites. However, these interactions are usually only computed between pairs of brain regions, at the risk of missing simultaneous interactions of three or more areas, an aspect that is crucial in a networked disease such as TLE. We thus propose to track, on a rich dataset of electrophysiological brain signals recorded within the TL of adult male Wistar Han rats, the formation and dissolution of high-order informational multiplets in time during distinct natural behaviors in an animal model of TLE. We identified the informational content of the multiplets as synergistic or redundant. Results identified an early transition of synergistic and redundant multiplets ahead of TLE onset with the predominant involvement of four TL brain regions in generating theta (4-12 Hz) activity. This shift has been shown predominantly during exploration, a theta-dependent behavior, less during rest and sleep. This specific change suggests a shift in communication from an integrated to a segregated network toward TLE onset.</jats:p><jats:p><jats:bold>Significance Statement</jats:bold>Temporal lobe epilepsy (TLE) is a prevalent network disorder that is often pharmacoresistant; therefore, TLE prevention is critical. This research article identifies early signs of TLE by studying collective dynamics within the TL using an information decomposition technique during natural behaviors. This computational method, beyond pairwise interactions, may thus need to be used to identify early biomarkers for TLE onset.}},
  articleno    = {{ENEURO.0403-24.2025}},
  author       = {{Mirjebreili, Morteza and Martinez de Aguirre Ibarreta, Josu and Marinazzo, Daniele and Chauvière, Laetitia}},
  issn         = {{2373-2822}},
  journal      = {{ENEURO}},
  keywords     = {{epilepsy,information theory,computational neuroscience,signal processing,complex systems,animal study,electrophysiology in vivo,epileptogenesis,higher-order interactions,prediction,temporal lobe epilepsy,BRAIN INSULTS,THETA RHYTHM,INTEGRATION,SEQUENCES,ONSET}},
  language     = {{eng}},
  number       = {{5}},
  pages        = {{27}},
  title        = {{High-order information analysis of epileptogenesis in the pilocarpine rat model of temporal lobe epilepsy}},
  url          = {{http://doi.org/10.1523/eneuro.0403-24.2025}},
  volume       = {{12}},
  year         = {{2025}},
}

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