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PreviousNext
Research ArticleResearch Article: New Research, Disorders of the Nervous System

High-Order Information Analysis of Epileptogenesis in the Pilocarpine Rat Model of Temporal Lobe Epilepsy

Morteza Mirjebreili, Josu Martinez de Aguirre Ibarreta, Daniele Marinazzo and Laetitia Chauvière
eNeuro 22 April 2025, 12 (5) ENEURO.0403-24.2025; https://doi.org/10.1523/ENEURO.0403-24.2025
Morteza Mirjebreili
1Institute for Cognitive Science Studies, Tehran 1658344575, Iran
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Josu Martinez de Aguirre Ibarreta
2Faculty of Engineering, Mondragon Unibertsitatea, Arrasate Mondragón 20500, Spain
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Daniele Marinazzo
3Department of Data Analysis, Ghent University, Ghent 9000, Belgium
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Laetitia Chauvière
4Institute for Molecular and Behavioral Neuroscience, University of Cologne, University Hospital Cologne, Cologne 50937, Germany
5INS - Institut de Neurosciences des Systèmes, UMR INSERM 1106, Aix-Marseille Université, Marseille 13385, France
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Figures

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  • Extended Data
  • Figure 1.
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    Figure 1.

    Impact of the data lengths of epochs on the mean number of interactions found per epoch of behavior. Examples of RED/SYN multiplets during sniffing (Extended Data Fig. 1-1 for multiplets during rest and sleep). This figure represents in the X axis the time points from D-7 (control stage, before injections) to D4, D7, D10, D14, and D25 post injections; in Y axis, the logarithmic of the lengths of epochs considered in our analysis to quantify the mean number of redundant and synergistic third-order interactions (triplets) at each time point, during sniffing in Category A (A) and Category B (B). This figure shows that, overall, the data lengths of the epochs considered in the analysis have no impact on the number of significant interactions found in those epochs. **p < 0.01 (only cases where data length significantly affects the number of HOIs found in the considered epochs). Note that for fourth-order HOIs (i.e., quadruplets), there is only zero or one HOI, as each category has four brain regions, thus the possibility of several third-order HOIs (triplets) but only one quadruplet. Nb. HOIs, number of HOIs.

  • Figure 2.
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    Figure 2.

    Examples of EEG traces for each brain region considered in the study. This figure depicts examples of EEG traces for each TL brain region considered in the present study before injections (at D-7, i.e., during the control stage), at D4 and D7 during sniffing behavior. X axis, time (in seconds); Y axis, amplitude (in millivolt). The scale is shown below each set of traces. See Extended Data Figures 2-1–2-5 for examples of EEG traces during sniffing at D10, D14 and D25, as well as during rest and sleep at all time points.

  • Figure 3.
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    Figure 3.

    Mean number of HOIs for third- and fourth-order redundant and synergistic multiplets, the total number of epochs considered in the analysis, and the total number of HOIs for each behavior and category during the control stage. These bar plots indicate the mean number of redundant (RED) triplets (RED 3), RED quadruplets (RED 4), synergistic (SYN) triplets (SYN 3), and SYN quadruplets (SYN 4), as well as the total number of HOIs for Category A (CAT A, left) and Category B (CAT B, right) in 100 epochs of sleep (in green), sniffing (SN, in blue), and rest (in red).

  • Figure 4.
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    Figure 4.

    Planar hypergraphs during natural behaviors. Those hypergraphs (cf. https://github.com/renzocom/hyperplot) depict graphical representations of redundant and synergistic triplets (Order 3) and quadruplets (Order 4) during sniffing (SN), rest, and sleep before model induction for Category A (A) and Category B (B).

  • Figure 5.
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    Figure 5.

    The mean number of redundant and synergistic multiplets during control versus epileptogenic stages for each behavior considered in the analysis. On the X axis are depicted the time points from the day before model induction (D-7, control stage) and the following days after model induction, namely, epileptogenic stages for experimental rats, both during the latent period (i.e., ahead of TLE onset, at D4, D7, and D10) and the chronic stage (i.e., epilepsy per se, at D14 and D25). Around D10–D14, on average, the experimental rats all developed their SZ1, marking TLE onset. On the Y axis are depicted the mean number of significant HOIs found in all epochs for all experimental rats. Plotted is the mean number of redundant or synergistic high-order TL multiplets along epileptogenesis compared with the control stage for two different orders of interactions (Order 3, triplets of TL brain regions; Order 4, quadruplets of TL brain regions). Those multiplets have been depicted in count plots for each order (3 and 4), where the radius of the circles is proportional to the mean number of interactions in Category A (A) and B (B). SYN 3, synergistic triplets (dark blue); SYN 4, synergistic quadruplets (light blue); RED 3, redundant triplets (dark red); RED 4, redundant quadruplets (light red). SN, sniffing.

  • Figure 6.
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    Figure 6.

    The mean number of HOIs along epileptogenic stages (D4, D7, and D10) compared with the control stage (D-7) for redundant and synergistic multiplets. This figure depicts the mean number of HOIs according to the four possible metrics: RED third order (dark red), RED fourth order (light red), SYN third order (dark blue), SYN fourth order (light blue) during the control stage (D-7) versus epileptogenic stages (D4 and D7) for both Category A (A) and B (B).

  • Figure 7.
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    Figure 7.

    Planar hypergraphs depicting the graphical representation of the evolution of HOIs from the control stage to the epileptogenic stages for sniffing behavior in each category. Extended Data Figure 7-1 for the same graphical representation during rest and sleep.

  • Figure 8.
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    Figure 8.

    Pearson's correlation plots between the number of redundant and synergistic multiplets during epileptogenesis. This figure depicts the Pearson's correlation between redundant and synergistic HOIs at each time point for all TL brain regions considered in the analysis and all behaviors in Category A (A) and Category B (B). X axis, the number of redundant HOIs; Y axis, the number of synergistic HOIs. A regression line indicates the correlation between redundant and synergistic HOIs for each plot, the p value the significance of this correlation, and the r coefficient the effect size. Nb. HOIs, number of HOIs. See Extended Data Figure 8-1 for the same graphical representation for each TL brain region considered in Category A (A) and Category B (B).

  • Figure 9.
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    Figure 9.

    Regional distribution of redundant and synergistic multiplets during control versus epileptogenic stages. These bar plots show the mean number and SD of HOIs at each time point for each brain region, behavior, and category: A, Category A; B, Category B. X axis, TL brain regions; Y axis, the mean number of HOIs.

  • Figure 10.
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    Figure 10.

    The mean number of redundant and synergistic multiplets during epileptogenic versus control stages in experimental animals for prominent high-order statistical interdependencies. These bar plots depict the mean number and SD of redundant and synergistic multiplets during epileptogenic stages versus the control stage (D-7) in experimental animals for prominent high-order triplets or quadruplets—per behavior and category, Category A (A) and Category B (B). X axis, specific HOIs; Y axis, the mean number of HOIs. SN, sniffing.

  • Figure 11.
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    Figure 11.

    Mean O-information along epileptogenesis compared with the control stage for redundant and synergistic multiplets involving each TL brain region during each behavior and category. Swarmplots of seaborn depicting the evolution of the distribution of the mean O-information values along epileptogenesis (from D4 to D25) compared with the control stage (D-7) during each behavior [sniffing (blue), rest (red), and sleep (green)], for redundant and synergistic multiplets involving a particular brain region according to Category A (A) or Category B (B).

  • Figure 12.
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    Figure 12.

    Mutual information between pairwise interactions of TL brain regions at each time point for each behavior and category. A, Heat maps depicting mutual information between all possible pairwise interactions at each time point for each behavior (sniffing, rest, and sleep) and category (A and B). Color bars have the same axis per behavior across time but different limits among behaviors, otherwise creating a loss of information. B, Swarmplots depicting the evolution of the distribution of the mutual information between pairwise interactions (involving a particular brain region) along epileptogenesis compared with the control stage (D-7) for each behavior and category.

  • Figure 13.
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    Figure 13.

    Comparison of the effect sizes of the changes in mutual information and O-information. Interaction information (equal to O-information for n = 3) already tells us how much information there is beyond mutual information. We were looking at mutual information to see whether we also observed some modulations over time when using it. We compared the effect sizes of the changes in the two quantities across time. For that, we computed the effect sizes of the changes in the five metrics, namely, mutual information (MI, black) and the four metrics of the O-information [RED third order (dark red), RED fourth order (light red), SYN third order (dark blue), and SYN fourth order (light blue)] along epileptogenesis, for each behavior and category (A, Category A; B, Category B). Note the absence of effect size for the SYN metrics (SYN 3 and SYN 4) during sleep in both categories since the Kruskal–Wallis test did not exhibit any significant change in O-information related to the control stage in both categories (thus, no post hoc tests were run).

Tables

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    Table 1.

    Histological results of electrode placement

    Rat number010203040506
    Brain regions
     MS✔✔ubt✔✔✔
     MS✔✔ubt✔✔✔
     Thal✔✔ubt✔✔✔
     SuM✔✔ubt✔✔✔
     dHPC✔✔ubt✔✔✔
     dHPC✔✔ubt✔✔✔
     dHPC✔✔ubt✔✔✔
     dHPC✔✔ubt✔✔✔
     vHPC✔✔ubt✔✔✔
     EC✔✔ubt✔✔✔
     EC✔✔ubt✔NA✔
    • This table presents the histological results (cresyl violet histology) of the electrode placement. “ubt,” unusable brain tissue; therefore histological procedures were unfortunately impossible to carry out; compare Materials and methods. NA, not applicable (lack of recording channel).

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    Table 2.

    Visual analysis of IA and ictal-like events (seizure activity) for each rat considered in the present study

    Rat number010203040506
    IA bursts typeIctal events (seizures, at D7 and at D10); Type B bursts (D7, D10)Type A IA (D7 and D10)Type A IA (D7); seizures at D10.Type A bursts (D7 and D10); Type 2 IA (Type B bursts, D10); ictal events (from D7)Type A bursts (D4, D7, and D10)Type A bursts (D4, D7 and D10)
    Brain regionsSeizure starting in the EC and propagating in all TL brain regions recorded (*); Type 2 IA in the hippocampus and ECSynchronized in all TL brain regions, inversion of polarity within dorsal hippocampal layers; EC; dHPC.EC; generalized seizures.Seizures usually start in the EC and propagating in all TL brain regions recordeda. Type 1 IA either synchronized EC–dHPC or independently occurring in the EC and/or in the dHPC (Type A bursts); Type 2 IA in the dHPCSynchronized in all TL brain regions, inversion of polarity within dorsal hippocampal layers; ECdHPC and vHPC
    • This analysis determines the type of IA bursts—based on the same features as the ones described in Chauvière et al. (2012)—and the seizure activity occurring along epileptogenic stages (namely, D4, D7, and D10), as well as which brain regions they involve. We note that Type B bursts occurred more prominently in two rats which have already undergone early seizure activity. The other rats have a similar pattern of (mainly Type A) IA bursts which characterizes a similar network trajectory along epileptogenesis.

    • ↵aPlus frontal cortex in case of generalized motor seizures.

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    Table 3.

    The total number of epochs and their corresponding number of redundant and synergistic third- or fourth-order multiplets for each behavior and category before injection (at D-7)

    Category A
    Sniffing
    Number of epochsTotal number of HOIs (regardless of their informational content)Number of significant RED HOIs (Order 3: triplets)Number of significant SYN HOIs (Order 3: triplets)Number of significant RED HOIs (Order 4: quadruplets)Number of significant SYN HOIs (Order 4: quadruplets)
    6452,5631,60353235078
    100397248825412
    Awake immobility
    3741,5961,07323127616
    10042628661734
    Sleep
    6330220142554
    10047931967876
    Category B
    Sniffing
    Number of epochsTotal number of HOIs (regardless of their informational content)Number of significant RED HOIs (Order 3: triplets)Number of significant SYN HOIs (Order 3: triplets)Number of significant RED HOIs (Order 4: quadruplets)Number of significant SYN HOIs (Order 4: quadruplets)
    6462,5931,69645740733
    10040126270635
    Awake immobility
    3741,5501,04123326511
    10041427862703
    Sleep
    6330218954554
    10047930085876
    • This table presents the total number of epochs considered in the analysis for each category and natural behavior—namely, sniffing, rest, and sleep—the total number of HOIs, also called multiplets, be it triplets (third-order multiplets) or quadruplets (fourth-order multiplets) and their informational content, redundant versus synergistic, per behavior and category considered in the analysis, during the control stage.

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    Table 4.

    The mean number of redundant (RED) and synergistic (SYN) multiplets during sniffing, rest, and sleep across time for Category A and Category B

    Category A
    SniffingRestSleep
    REDSYNREDSYNREDSYNREDSYNREDSYNREDSYN
    Third orderThird orderFourth orderFourth orderThird orderThird orderFourth orderFourth orderThird orderThird orderFourth orderFourth order
    D-72.2800.9850.3050.1552.4700.8460.5810.1033.4480.4140.7930.138
    D43.6030.2930.9310.0173.3660.4630.9270.0241.52.50.50
    D72.3480.7020.6240.0792.8820.5210.7560.0083.867010
    Category B
    SniffingRestSleep
    REDSYNREDSYNREDSYNREDSYNREDSYNREDSYN
    Third orderThird orderFourth orderFourth orderThird orderThird orderFourth orderFourth orderThird orderThird orderFourth orderFourth order
    D-71.7451.2550.3350.1252.6240.7610.5640.0343.1720.8280.8280.103
    D43.1690.6270.7630.0512.5371.0240.8540.0241.5210
    D72.9830.4380.75302.7230.4960.69703.7330.26710
    • This table presents the mean number of HOIs from the control stage (D-7) to epileptogenic stages (D4 and D7), highlighting a shift at D4 during sniffing, rest, and sleep, which is more prominent during sniffing in both categories. This number has been normalized by the number of epochs considered at each time point to allow for comparison.

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    Table 5.

    Pearson's correlation results between the number of redundant multiplets and the number of synergistic multiplets during epileptogenesis

    Category A
    BehaviorTime pointMSSuMdHPCEC
    prprprpr
    SleepD-70−0.9490−0.9650−0.950−0.958
    D4NANA1−11−11−1
    D7NANANANANANANANA
    D100.003−0.7070−0.9360−0.9360−1
    D251−11−1NANANANA
    SniffingD-70−0.5740−0.5830−0.5130−0.539
    D40−0.6790−0.7580−0.7180−0.652
    D70−0.6280−0.6260−0.6250−0.629
    D100−0.7440−0.720−0.740−0.795
    D140−0.7420−0.8290−0.7270−0.82
    D250.004−0.5980.001−0.650.005−0.5870.001−0.681
    RestD-70−0.6670−0.6360−0.5340−0.683
    D40−0.6990−0.6980−0.7060−0.722
    D70−0.6280−0.6510−0.5030−0.64
    D100−0.8210−0.690−0.680−0.671
    D140−10−10−10−1
    D250.389−0.250.105−0.4520.011−0.6550.461−0.215
    Category B
    BehaviorTime pointMSSuMdHPCEC
    prprprpr
    SleepD-70−0.8880−0.8490−0.8560−0.856
    D4NANANANANANANANA
    D70−10−10−10−1
    D100.006−0.6750.215−0.340.025−0.5740.035−0.548
    D251−11−11−11−1
    SniffingD70−0.6110−0.6010−0.6360−0.625
    D40−0.8820−0.8060−0.8530−0.787
    D70−0.5730−0.4230−0.6240−0.6
    D100−0.6450−0.5330−0.5960−0.555
    D140−0.6250−0.6390.006−0.450−0.6
    D250.003−0.6350.003−0.6350.009−0.5670.054−0.436
    RestD-70−0.6430−0.6280−0.6070−0.511
    D40−0.8560−0.7390−0.7410−0.78
    D70−0.5530−0.6360−0.5610−0.623
    D100−0.8880−0.8190−0.8360−0.841
    D14NANANANANANANANA
    D250.055−0.5440.045−0.5630.055−0.5440.068−0.52
    • This table shows the results from Pearson's correlation between the number of redundant multiplets and the number of synergistic multiplets at each time point for each behavior, category, and each TL brain region considered in our analysis. p stands for p value, and r stands for correlation coefficient (also stands for the effect size). NA, not applicable. NA values stand for undefined r values, which typically occur when one or both variables (namely, either #RED or #SYN) exhibit zero variance. Specifically, Pearson's correlation coefficient is undefined when at least one of the variables has a constant value, resulting in zero SD. The formula to calculate r involves dividing by the product of SD of #RED (SD1) and of #SYN (SD2); thus when the SD of one of the variables is zero, the denominator of the formula becomes zero, leading to an undefined or NaN result (NA value).

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    Table 6.

    Summary of p values and effect sizes (ES) for redundant and synergistic multiplets

    CategoryBehaviorTypeOrderTime pointp valueES
    ASniffingRedundantTripletsD4<0.0011.119
    ASniffingRedundantTripletsD710.053
    ASniffingRedundantTripletsD100.0570.264
    ASniffingRedundantTripletsD1410.041
    ASniffingRedundantTripletsD250.4870.454
    ASniffingRedundantQuadrupletsD4<0.0011.475
    ASniffingRedundantQuadrupletsD7<0.0010.673
    ASniffingRedundantQuadrupletsD10<0.0010.76
    ASniffingRedundantQuadrupletsD140.380.298
    ASniffingRedundantQuadrupletsD2510.097
    ASniffingSynergisticTripletsD4<0.0010.773
    ASniffingSynergisticTripletsD100.0830.162
    ASniffingSynergisticTripletsD1410.074
    ASniffingSynergisticTripletsD250.7150.478
    ASniffingSynergisticQuadrupletsD40.0400.423
    ASniffingSynergisticQuadrupletsD70.1860.237
    ASniffingSynergisticQuadrupletsD1010.108
    ASniffingSynergisticQuadrupletsD140.0050.537
    ASniffingSynergisticQuadrupletsD2510.298
    ARestRedundantTripletsD40.0020.619
    ARestRedundantQuadrupletsD4<0.0010.772
    ASleepRedundantTripletsD40.0201.757
    ASleepSynergisticTripletsD40.0082.542
    BSniffingRedundantTripletsD4<0.0010.966
    BSniffingRedundantTripletsD7<0.0010.862
    BSniffingRedundantTripletsD10<0.0010.909
    BSniffingRedundantTripletsD14<0.0011.256
    BSniffingRedundantTripletsD2510.061
    BSniffingRedundantQuadrupletsD4<0.0010.923
    BSniffingRedundantQuadrupletsD7<0.0010.919
    BSniffingRedundantQuadrupletsD10<0.0011.041
    BSniffingRedundantQuadrupletsD14<0.0011.222
    BSniffingRedundantQuadrupletsD2510.032
    BSniffingSynergisticTripletsD4<0.0010.546
    BSniffingSynergisticTripletsD7<0.0010.792
    BSniffingSynergisticTripletsD10<0.0010.818
    BSniffingSynergisticTripletsD14<0.0011.028
    BSniffingSynergisticTripletsD2510.037
    BSniffingSynergisticQuadrupletsD7<0.0010.518
    BSniffingSynergisticQuadrupletsD10<0.0010.429
    BSniffingSynergisticQuadrupletsD140.0170.409
    BSniffingSynergisticQuadrupletsD2510.075
    BRestRedundantTripletsD140.0350.932
    BRestRedundantQuadrupletsD40.0050.621
    BRestRedundantQuadrupletsD100.0010.569
    BRestRedundantQuadrupletsD140.0390.909
    BSleepRedundantTripletsD100.0160.83
    • This table presents the statistics corresponding Results, Early shift of redundant and synergistic multiplets during epileptogenesis. To avoid disrupting the flow of reading, we did not want to clutter the main text with statistics. Instead we decided to include them in a separate table as they included both p values and effect sizes.

    • View popup
    Table 7.

    The mean number of redundant and synergistic triplets and quadruplets during epileptogenic versus control stages in experimental animals for prominent high-order interdependencies

    Category A
    BehaviorTime pointMS, Thal, vHPCMS, Thal, dHPCThal, dHPC, vHPCMS, dHPC, vHPCMS, Thal, dHPC, vHPC
    REDSYNREDSYNREDSYNREDSYNREDSYN
    SleepD-70.8970.0690.8620.1030.8970.1030.7930.1380.7930.138
    D410010.50.5010.50
    D71010100.867010
    D1010100.3330.6670.20.66710
    D2500.50.50.5010.50.50.50
    SniffingD-70.6260.1380.2860.5810.6750.1480.660.1030.30.153
    D40.8810.0680.9150.0510.8640.0850.8810.0850.9150.017
    D70.570.1280.6030.2510.4750.2230.6870.0950.620.078
    D100.7790.1230.5320.3180.5190.2790.7790.0970.6560.117
    D140.6940.1390.4440.4720.4440.4170.750.0280.4440.361
    D250.4760.3330.2380.5240.4290.3810.4760.1430.3330.048
    RestD-70.6330.1750.50.3330.5920.20.6830.1170.5670.1
    D40.8330.1190.810.1190.810.0950.8330.1190.9050.024
    D70.7080.1330.8170.1250.60.1670.7330.0920.750.008
    D100.8670.0930.760.1470.7070.080.7730.1470.8130.027
    D140.90.1100.90.1100.90
    D250.7860.0710.2140.5710.7140.2140.5710.1430.7140
    Category B
    BehaviorTime pointMS, SuM, dHPCEC, MS, SuMEC, MS, dHPCEC, SuM, dHPCEC, MS, SuM, dHPC
    REDSYNREDSYNREDSYNREDSYNREDSYN
    SleepD-70.7670.20.7670.20.70.2670.8330.1330.80.793
    D401010.501010.5
    D7100.8670.133100.8670.13311
    D10100.2670.5330.20.6670.6670.1330.8671
    D250.50.50.50.510100.50.5
    SniffingD70.2960.4240.4630.2170.4580.310.5020.2860.330.3
    D40.8640.1360.7460.1860.7460.1860.8140.1190.7630.915
    D70.9330.0110.7810.0620.6350.2250.6350.140.7530.62
    D100.7710.1110.7780.0920.7520.1240.7450.0720.7970.656
    D140.9170.0280.8890.0560.8610.0280.94400.8890.444
    D250.40.50.250.40.50.250.50.150.350.333
    RestD-70.60.2420.650.20.6420.1670.6670.1330.550.567
    D40.8540.1220.4880.3660.5610.3170.6340.220.8540.905
    D70.9160.0250.5880.2350.5880.0760.630.160.6970.75
    D100.8650.0810.770.1620.6760.2030.8380.0810.8240.813
    D140.9010101010.9
    D250.3850.0770.7690.0770.6920.0770.7690.0770.7690.714
    • This table shows the mean number of redundant and synergistic triplets and quadruplets at each time point, for each behavior and category (A and B).

    • View popup
    Table 8.

    Shift in redundant and synergistic multiplets related to the day of the SZ1 of all experimental rats considered in the analysis

    Rat numberSZ1SNIFFINGRESTSLEEP
    Category ACategory BCategory ACategory BCategory ACategory B
    REDSYNREDSYNREDSYNREDSYNREDSYNREDSYN
    01D8NSNSNSNSNSNSNSD10NSNSNSNS
    02>D10D14D7NSNSNSNSNSNSNSNSNSNS
    03D10D4D7D7D7NSNSNSNSNSNSNSNS
    04D7D10D7D10D10NSNSNSNSD10D10NSNS
    05>D10D4D4D4D4D4D4D7NSNSNSD7D7
    06>D10NSNSNSNSNSNSNSD25NSNSNSNS
    • Significant shift in redundant (RED) and synergistic (SYN) multiplets during each behavior (sniffing, rest, or sleep), for each category (A or B) and experimental rat related to the day of their SZ1 to investigate whether an early shift in the informational content of higher-order interactions could be predictive of an early occurrence of SZ1, thus of an early TLE onset. NS, not significant. D7 is considered an early SZ1, D10 a standard SZ1, and >D10 a late SZ1.

Extended Data

  • Figures
  • Tables
  • Figure 1-1

    Impact of the data lengths of epochs on the mean number of interactions found per epoch of behavior for remaining multiplets and behaviors. This figure is an extension of Figure 1 for the remaining multiplets and behaviors in both categories. This figure thus represents in the X axis the time points from D-7 (control stage, before injections) to D4, D7, D10, D14, and D25 post injections, in the Y axis, the logarithmic of the lengths of epochs considered in our analysis to quantify the number of redundant and synergistic multiplets at each time point, during rest and sleep in Category A (A) and Category B (B). As in Figure 1, this figure shows that, overall, the data length of the epochs considered in the analysis has no impact on the number of significant interactions found in those epochs. **: p < 0.01 (only cases where data length significantly affects the number of HOIs found in the considered epochs). Nb HOIs: Number of HOIs. Download Figure 1-1, TIF file.

  • Figure 2-1

    Examples of EEG traces. As an extension of Figure 2, this figure depicts examples of EEG traces for each TL brain region considered in the present study at D10, D14, and D25 during sniffing behavior. X axis: time (in sec); Y axis: amplitude (in mV). The scale is shown below each set of traces. Download Figure 2-1, TIF file.

  • Figure 2-2

    Examples of EEG traces. As an extension of Figure 2, this figure depicts examples of EEG traces for each TL brain region considered in the present study at D-7 (control stage), D4, and D7 during rest behavior (awake immobility). X axis: time (in sec); Y axis: amplitude (in mV). The scale is shown below each set of traces. Download Figure 2-2, TIF file.

  • Figure 2-3

    Examples of EEG traces. As an extension of Figure 2, this figure depicts examples of EEG traces for each TL brain region considered in the present study at D10, D14, and D25 during rest behavior (awake immobility). X axis: time (in sec); Y axis: amplitude (in mV). The scale is shown below each set of traces. Download Figure 2-3, TIF file.

  • Figure 2-4

    Examples of EEG traces. As an extension of Figure 2, this figure depicts examples of EEG traces for each TL brain region considered in the present study at D-7 (control stage), D4, and D7 during sleep behavior (slow wave sleep). X axis: time (in sec); Y axis: amplitude (in mV). The scale is shown below each set of traces. Download Figure 2-4, TIF file.

  • Figure 2-5

    Examples of EEG traces. As an extension of Figure 2, this figure depicts examples of EEG traces for each TL brain region considered in the present study at D10 and D25 during sleep behavior (slow wave sleep). Note the absence of epochs at D14 during sleep. X axis: time (in sec); Y axis: amplitude (in mV). The scale is shown below each set of traces. Download Figure 2-5, TIF file.

  • Figure 7-1

    Planar hypergraphs during rest and sleep depicting the evolution of the mean number of interactions from the control to epileptogenic stages. Those hypergraphs depict the graphical representation of the evolution of HOIs from the control stage to the epileptogenic stages during rest and sleep in Category A (CAT A) and Category B (CAT B), extending Figure 5C, which depicts similar planar hypergraphs during sniffing. Download Figure 7-1, TIF file.

  • Figure 8-1

    Pearson’s correlation plots between the number of redundant and synergistic multiplets during epileptogenesis. This figure depicts Pearson’s correlation between redundant and synergistic HOIs at each time point for each TL brain region and all behaviors in Category A (A) and Category B (B). X axis: number of redundant HOIs, Y axis: number of synergistic HOIs. A regression line indicates the correlation between redundant and synergistic HOIs for each plot, the p-value indicates the significance of this correlation, and the r coefficient (Pearson’s correlation coefficient) indicates the effect size. Nb. HOIs: Number of HOIs. Download Figure 8-1, TIF file.

  • Figure 9-1

    Statistics corresponding to the third section of the Results entitled “Regional distribution of redundant and synergistic multiplets during epileptogenesis”. Download Figure 9-1, DOC file.

  • Figure 10-1

    Statistics corresponding to the fourth section of the Results entitled “Evolution of triplets and quadruplets during epileptogenesis”. Download Figure 10-1, DOC file.

  • Figure 11-1

    Statistics corresponding to the fifth section of the Results entitled “Dynamics of O-information along epileptogenesis”. Download Figure 11-1, DOC file.

  • Figure 12-1

    Statistics corresponding to the mutual information discussed in the sixth section of the Results entitled “Added value of higher-order interactions”. Download Figure 12-1, DOC file.

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High-Order Information Analysis of Epileptogenesis in the Pilocarpine Rat Model of Temporal Lobe Epilepsy
Morteza Mirjebreili, Josu Martinez de Aguirre Ibarreta, Daniele Marinazzo, Laetitia Chauvière
eNeuro 22 April 2025, 12 (5) ENEURO.0403-24.2025; DOI: 10.1523/ENEURO.0403-24.2025

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High-Order Information Analysis of Epileptogenesis in the Pilocarpine Rat Model of Temporal Lobe Epilepsy
Morteza Mirjebreili, Josu Martinez de Aguirre Ibarreta, Daniele Marinazzo, Laetitia Chauvière
eNeuro 22 April 2025, 12 (5) ENEURO.0403-24.2025; DOI: 10.1523/ENEURO.0403-24.2025
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  • animal study
  • electrophysiology in vivo
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