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Diurnal rhythms of spontaneous intracranial high-frequency oscillations

  • Gabrielle T. Petito
    Affiliations
    Comprehensive Epilepsy Center, Division of Neurology, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio, USA
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  • Jeremy Housekeeper
    Affiliations
    Comprehensive Epilepsy Center, Division of Neurology, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio, USA
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  • Jason Buroker
    Affiliations
    Comprehensive Epilepsy Center, Division of Neurology, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio, USA
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  • Craig Scholle
    Affiliations
    Comprehensive Epilepsy Center, Division of Neurology, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio, USA
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  • Brian Ervin
    Affiliations
    Comprehensive Epilepsy Center, Division of Neurology, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio, USA

    Department of Electrical Engineering and Computer Science, University of Cincinnati, Cincinnati, Ohio, USA
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  • Clayton Frink
    Affiliations
    Comprehensive Epilepsy Center, Division of Neurology, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio, USA
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  • Hansel M. Greiner
    Affiliations
    Comprehensive Epilepsy Center, Division of Neurology, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio, USA

    Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, Ohio, USA
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  • Jesse Skoch
    Affiliations
    Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, Ohio, USA

    Division of Pediatric Neurosurgery, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio, USA
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  • Francesco T. Mangano
    Affiliations
    Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, Ohio, USA

    Division of Pediatric Neurosurgery, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio, USA
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  • Thomas J. Dye
    Affiliations
    Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, Ohio, USA

    Sleep Center, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio, USA.
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  • John B. Hogenesch
    Affiliations
    Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, Ohio, USA

    Circadian Biology Lab, Division of Human Genetics, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio, USA
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  • Tracy A. Glauser
    Affiliations
    Comprehensive Epilepsy Center, Division of Neurology, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio, USA

    Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, Ohio, USA
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  • Katherine D. Holland
    Affiliations
    Comprehensive Epilepsy Center, Division of Neurology, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio, USA

    Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, Ohio, USA
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  • Ravindra Arya
    Correspondence
    Corresponding author at: Division of Neurology, Cincinnati Children's Hospital Medical Center, 3333 Burnet Avenue, MLC 2015, Cincinnati, Ohio, USA 45229.
    Affiliations
    Comprehensive Epilepsy Center, Division of Neurology, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio, USA

    Department of Electrical Engineering and Computer Science, University of Cincinnati, Cincinnati, Ohio, USA

    Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, Ohio, USA
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Published:September 28, 2022DOI:https://doi.org/10.1016/j.seizure.2022.09.019

      Highlights

      • Intracranial high-frequency oscillations (HFOs) show a significant diurnal rhythm.
      • Diurnal rhythm of HFOs is relatively attenuated within the seizure-onset zone (SOZ).
      • Peak difference in HFO density within/outside SOZ consistently precedes seizures.
      • Difference in HFO density within/outside SOZ peaks at 1st hour after arousal and ±2 hours around sleep onset.

      Abstract

      Objective

      Seizures are known to occur with diurnal and other rhythms. To gain insight into the neurophysiology of periodicity of seizures, we tested the hypothesis that intracranial high-frequency oscillations (HFOs) show diurnal rhythms and sleep-wake cycle variation. We further hypothesized that HFOs have different rhythms within and outside the seizure-onset zone (SOZ).

      Methods

      In drug-resistant epilepsy patients undergoing stereotactic-EEG (SEEG) monitoring to localize SOZ, we analyzed the number of 50-200 Hz HFOs/channel/minute (HFO density) through a 24-hour period. The distribution of HFO density during the 24-hour period as a function of the clock time was analyzed with cosinor model, and for non-uniformity with the sleep-wake cycle.

      Results

      HFO density showed a significant diurnal rhythm overall and both within and outside SOZ. This diurnal rhythm of HFO density showed significantly lower amplitude and longer acrophase within SOZ compared to outside SOZ. The peaks of difference in HFO density within and outside SOZ preceded the seizures by approximately 4 hours. The difference in HFO density within and outside SOZ also showed a non-uniform distribution as a function of sleep-wake cycle, with peaks at first hour after arousal and ±2 hours around sleep onset.

      Conclusions

      Our study shows that the diurnal rhythm of intracranial HFOs is more robust outside the SOZ. This suggests cortical tissue within SOZ generates HFOs relatively more uniformly throughout the day with attenuation of expected diurnal rhythm. The difference in HFO density within and outside SOZ also showed non-uniform distribution according to clock times and the sleep-wake cycle, which can be a potential biomarker for preferential times of pathological cortical excitability. A temporal correlation with seizure occurrence further substantiates this hypothesis.

      Keywords

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      References

      1. Zarowski M, Loddenkemper T, Vendrame M, Alexopoulos AV, Wyllie E, Kothare SV. Circadian distribution and sleep/wake patterns of generalized seizures in children Epilepsia. 2011 Jun;52:1076-1083.

      2. Loddenkemper T, Vendrame M, Zarowski M, Gregas M, Alexopoulos AV, Wyllie E, et al. Circadian patterns of pediatric seizures Neurology. 2011 Jan 11;76:145-153.

        • Gurkas E
        • Serdaroglu A
        • Hirfanoglu T
        • Kartal A
        • Yilmaz U
        • Bilir E.
        Sleep-wake distribution and circadian patterns of epileptic seizures in children European journal of paediatric neurology.
        EJPN. 2016; 20 (Jul): 549-554
      3. Unterberger I, Gabelia D, Prieschl M, Chea K, Hofer M, Hogl B, et al. Sleep disorders and circadian rhythm in epilepsy revisited: a prospective controlled study Sleep medicine. 2015 Feb;16:237-242.

        • Karoly PJ
        • Goldenholz DM
        • Freestone DR
        • Moss RE
        • Grayden DB
        • Theodore WH
        • et al.
        Circadian and circaseptan rhythms in human epilepsy.
        Retrospect Cohort Study Lancet Neurol. 2018; 17 (Nov): 977-985
        • van Campen JS
        • Valentijn FA
        • Jansen FE
        • Joels M
        • Braun KP.
        Seizure occurrence and the circadian rhythm of cortisol.
        System Rev Epilepsy Behav: E&B. 2015; 47 (Jun): 132-137
      4. Ly JQM, Gaggioni G, Chellappa SL, Papachilleos S, Brzozowski A, Borsu C, et al. Circadian regulation of human cortical excitability Nature communications. 2016 Jun 24;7:11828.

      5. Leguia MG, Andrzejak RG, Rummel C, Fan JM, Mirro EA, Tcheng TK, et al. Seizure Cycles in Focal Epilepsy JAMA neurology. 2021 Apr 1;78:454-463.

      6. Frauscher B, von Ellenrieder N, Zelmann R, Rogers C, Nguyen DK, Kahane P, et al. High-Frequency Oscillations in the Normal Human Brain Annals of neurology. 2018 Sep;84:374-385.

        • Engel Jr., J
        • Bragin A
        • Staba R
        • Mody I
        High-frequency oscillations: what is normal and what is not?.
        Epilepsia. 2009; 50 (Apr): 598-604
        • Kucewicz MT
        • Cimbalnik J
        • Matsumoto JY
        • Brinkmann BH
        • Bower MR
        • Vasoli V
        • et al.
        High frequency oscillations are associated with cognitive processing in human recognition memory Brain.
        J Neurol. 2014; 137 (Aug): 2231-2244
        • Jiruska P
        • Powell AD
        • Chang WC
        • Jefferys JG.
        Electrographic high-frequency activity and epilepsy.
        Epilepsy Res. 2010 Mar; 89: 60-65
      7. Navarrete M, Alvarado-Rojas C, Le Van Quyen M, Valderrama M. RIPPLELAB: A Comprehensive Application for the Detection, Analysis and Classification of High Frequency Oscillations in Electroencephalographic Signals PloS one. 2016;11:e0158276.

        • Zelmann R
        • Mari F
        • Jacobs J
        • Zijlmans M
        • Dubeau F
        • Gotman J.
        A comparison between detectors of high frequency oscillations Clinical neurophysiology:.
        Off J Int Federation Clin Neurophysiol. 2012 Jan; 123: 106-116
        • Zelmann R
        • Mari F
        • Jacobs J
        • Zijlmans M
        • Chander R
        • Gotman J.
        Automatic detector of high frequency oscillations for human recordings with macroelectrodes Conference proceedings.
        in: Annual International Conference of the IEEE Engineering in Medicine and Biology Society IEEE Engineering in Medicine and Biology Society Conference. 2010. 2010: 2329-2333
        • Chander R.
        Algorithms to detect high frequency oscillations in human intracerebral EEG.
        McGill University, 2007
      8. Nelson W, Tong YL, Lee JK, Halberg F. Methods for cosinor-rhythmometry Chronobiologia. 1979 Oct-Dec;6:305-323.

      9. Cornelissen G. Cosinor-based rhythmometry Theoretical biology & medical modelling. 2014 Apr 11;11:16.

      10. Sachs M. Package ‘cosinor’. 1.1 ed2014.

        • Kuroda N
        • Sonoda M
        • Miyakoshi M
        • Nariai H
        • Jeong JW
        • Motoi H
        • et al.
        Objective interictal electrophysiology biomarkers optimize prediction of epilepsy surgery outcome.
        Brain Commun. 2021; 3 (fcab042)
      11. Nagasawa T, Juhasz C, Rothermel R, Hoechstetter K, Sood S, Asano E. Spontaneous and visually driven high-frequency oscillations in the occipital cortex: intracranial recording in epileptic patients Hum Brain Mapp. 2012 Mar;33:569-583.

        • Matsumoto A
        • Brinkmann BH
        • Matthew Stead S
        • Matsumoto J
        • Kucewicz MT
        • Marsh WR
        • et al.
        Pathological and physiological high-frequency oscillations in focal human epilepsy.
        J Neurophysiol. 2013 Oct; 110: 1958-1964
        • Bagshaw AP
        • Jacobs J
        • LeVan P
        • Dubeau F
        • Gotman J.
        Effect of sleep stage on interictal high-frequency oscillations recorded from depth macroelectrodes in patients with focal epilepsy.
        Epilepsia. 2009 Apr; 50: 617-628
        • Spencer DC
        • Sun FT
        • Brown SN
        • Jobst BC
        • Fountain NB
        • Wong VS
        • et al.
        Circadian and ultradian patterns of epileptiform discharges differ by seizure-onset location during long-term ambulatory intracranial monitoring.
        Epilepsia. 2016 Sep; 57: 1495-1502
        • Malow BA
        • Lin X
        • Kushwaha R
        • Aldrich MS.
        Interictal spiking increases with sleep depth in temporal lobe epilepsy.
        Epilepsia. 1998 Dec; 39: 1309-1316
        • Pavlova MK
        • Shea SA
        • Scheer FA
        • Bromfield EB.
        Is there a circadian variation of epileptiform abnormalities in idiopathic generalized epilepsy?.
        Epilepsy Behav: E&B. 2009 Nov; 16: 461-467
      12. Herman ST, Walczak TS, Bazil CW. Distribution of partial seizures during the sleep–wake cycle: differences by seizure onset site Neurology. 2001 Jun 12;56:1453-1459.

        • Bazil CW
        • Walczak TS.
        Effects of sleep and sleep stage on epileptic and nonepileptic seizures.
        Epilepsia. 1997 Jan; 38: 56-62
      13. Agostini A, Centofanti S. Normal Sleep in Children and Adolescence Child and adolescent psychiatric clinics of North America. 2021 Jan;30:1-14.

        • Quigg M.
        Circadian rhythms: interactions with seizures and epilepsy.
        Epilepsy Res. 2000 Nov; 42: 43-55
      14. Khan S, Nobili L, Khatami R, Loddenkemper T, Cajochen C, Dijk DJ, et al. Circadian rhythm and epilepsy Lancet neurology. 2018 Dec;17:1098-1108.

        • Melani F
        • Zelmann R
        • Mari F
        • Gotman J.
        Continuous High Frequency Activity: a peculiar SEEG pattern related to specific brain regions Clinical neurophysiology.
        Off J Int Federation Clin Neurophysiol. 2013 Aug; 124: 1507-1516
      15. Li G, Jiang S, Paraskevopoulou SE, Wang M, Xu Y, Wu Z, et al. Optimal referencing for stereo-electroencephalographic (SEEG) recordings NeuroImage. 2018 Dec;183:327-335.

        • Mitsuhashi T
        • Sonoda M
        • Iwaki H
        • Luat AF
        • Sood S
        • Asano E.
        Effects of depth electrode montage and single-pulse electrical stimulation sites on neuronal responses and effective connectivity Clinical neurophysiology.
        Off J Int Federation Clin Neurophysiol. 2020 Dec; 131: 2781-2792
      16. Gliske SV, Irwin ZT, Chestek C, Hegeman GL, Brinkmann B, Sagher O, et al. Variability in the location of high frequency oscillations during prolonged intracranial EEG recordings Nature communications. 2018 Jun 1;9:2155.

        • Reed CM
        • Birch KG
        • Kaminski J
        • Sullivan S
        • Chung JM
        • Mamelak AN
        • et al.
        Automatic detection of periods of slow wave sleep based on intracranial depth electrode recordings.
        J Neurosci Methods. 2017 Apr 15; 282: 1-8
        • von Ellenrieder N
        • Peter-Derex L
        • Gotman J
        • Frauscher B.
        SleepSEEG: automatic sleep scoring using intracranial EEG recordings only.
        J Neural Eng. 2022 May 3; : 19
        • Wang Y
        • Yuan L
        • Zhang S
        • Liang S
        • Yu X
        • Liu T
        • et al.
        Fast Ripples as a Biomarker of Epileptogenic Tuber in Tuberous Sclerosis Complex Patients Using Stereo-Electroencephalograph Frontiers in human neuroscience.
        Original Res. 2021; 15
        • Cuello-Oderiz C
        • von Ellenrieder N
        • Sankhe R
        • Olivier A
        • Hall J
        • Dubeau F
        • et al.
        Value of ictal and interictal epileptiform discharges and high frequency oscillations for delineating the epileptogenic zone in patients with focal cortical dysplasia Clinical neurophysiology.
        Off J Int Federation Clin Neurophysiol. 2018 Jun; 129: 1311-1319
        • Brazdil M
        • Halamek J
        • Jurak P
        • Daniel P
        • Kuba R
        • Chrastina J
        • et al.
        Interictal high-frequency oscillations indicate seizure onset zone in patients with focal cortical dysplasia.
        Epilepsy Res. 2010 Jun; 90: 28-32
        • Li P
        • Fu X
        • Smith NA
        • Ziobro J
        • Curiel J
        • Tenga MJ
        • et al.
        Loss of CLOCK Results in Dysfunction of Brain Circuits Underlying Focal.
        Epilepsy Neuron. 2017 Oct 11; 96 (e386): 387-401
      17. Lipton JO, Yuan ED, Boyle LM, Ebrahimi-Fakhari D, Kwiatkowski E, Nathan A, et al. The Circadian Protein BMAL1 Regulates Translation in Response to S6K1-Mediated Phosphorylation Cell. 2015 May 21;161:1138-1151.