Advertisement

Dynamics of seizure-induced behavioral and autonomic arousal

  • Emilia Toth
  • Ganne Chaitanya
  • Michael Pogwizd
  • Diana Pizarro
  • Adeel Ilyas
  • Steven Pogwizd
  • Sandipan Pati
Research Article

Abstract

Purpose

Arousal is the most primitive, powerful instinct with survival benefit present in all vertebrates. Even though the arousal systems are classically viewed as “ascending” brainstem phenomena, there is a “descending” cortical feedback system that maintains consciousness. In this study, we provide electrophysiological confirmation that seizures localized to the anterior cingulum can behaviorally manifest as paroxysms of arousal from sleep.

Methods

Temporal dynamics of arousal induced by anterior cingulate seizures were analyzed by using multiple modalities including stereoelectroencephalography (phase lag index and phase amplitude coupling), lead-1 ECG (point-process heart rate variability analysis) and diffusion tractography (DTI).

Results

The ictal arousal was associated with an increase in synchronization in the alpha band and an increase in local theta or alpha-gamma phase-amplitude coupling. In comparison to seizures that lacked clinical manifestations, ictal arousal was associated with an increase in heart rate but not heart rate variability. Finally, DTI demonstrated degeneration in white fiber tracts passing between the anterior cingulum and anterior thalamus ipsilateral to the epileptogenic cortex. The patient underwent resection of the anterior cingulum, and histopathology confirmed focal cortical dysplasia type II.

Conclusion

Anterior cingulate seizures inducing behavioral arousal have identifiable autonomic and EEG signatures.

Keywords

Arousal Hypnopompic seizure Anterior cingulate Phase lag index Phase-amplitude coupling Heart rate variability 

Notes

Author Contributions

SP was instrumental in the conception and design of the study, evaluation of the patient and EMU acquisition of data, contributed to data analysis and writing the manuscript. ET and GC performed analysis and interpretation of data and drafting the article or revising it critically for important intellectual content. MPo and SPo were instrumental in the analysis of HR and HRV. DP and AI helped in data collection, timely critical review of the results and concepts and in the revision of the manuscript. SP in the capacity of the corresponding author agrees to be accountable for all aspects of the work in ensuring the accuracy or integrity of any part of the work investigated and resolved.

Funding

Emilia Toth, Diana Pizarro, and SP gratefully acknowledge support from the USA National Science Foundation (NSF RII-2 FEC OIA1632891).

Compliance with Ethical Standards

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Supplementary material

10286_2018_543_MOESM1_ESM.docx (2.3 mb)
Supplementary material 1 (DOCX 2309 kb)

References

  1. 1.
    Malow BA (2007) The interaction between sleep and epilepsy. Epilepsia 48(Suppl 9):36–38CrossRefPubMedGoogle Scholar
  2. 2.
    Bonnet MH et al (1992) EEG scoring rules and examples: a preliminary report from the Sleep Disorders Atlas Task Force of the American Sleep Disorders Association. Sleep 15(2):173–184CrossRefGoogle Scholar
  3. 3.
    Awad AM, Luders HO (2010) Hypnopompic seizures. Epileptic Disord 12(4):270–274PubMedGoogle Scholar
  4. 4.
    Vetrugno R, Mascalchi M, Vella A, Della Nave R, Provini F, Plazzi G, Volterrani D, Bertelli P, Vattimo A, Lugaresi E et al (2005) Paroxysmal arousal in epilepsy associated with cingulate hyperperfusion. Neurology 64(2):356–358CrossRefPubMedGoogle Scholar
  5. 5.
    Stam CJ, Nolte G, Daffertshofer A (2007) Phase lag index: assessment of functional connectivity from multi channel EEG and MEG with diminished bias from common sources. Hum Brain Mapp 28(11):1178–1193CrossRefPubMedGoogle Scholar
  6. 6.
    Tort AB, Komorowski R, Eichenbaum H, Kopell N (2010) Measuring phase-amplitude coupling between neuronal oscillations of different frequencies. J Neurophysiol 104(2):1195–1210CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Barbieri R, Brown EN (2006) Analysis of heartbeat dynamics by point process adaptive filtering. IEEE Trans Bio-med Eng 53(1):4–12CrossRefGoogle Scholar
  8. 8.
    Kompanje EJ (2008) The devil lay upon her and held her down. Hypnagogic hallucinations and sleep paralysis described by the Dutch physician Isbrand van Diemerbroeck (1609–1674) in 1664. J Sleep Res 17(4):464–467CrossRefPubMedGoogle Scholar
  9. 9.
    Critchley HD, Mathias CJ, Josephs O, O’Doherty J, Zanini S, Dewar BK, Cipolotti L, Shallice T, Dolan RJ (2003) Human cingulate cortex and autonomic control: converging neuroimaging and clinical evidence. Brain 126(Pt 10):2139–2152CrossRefPubMedGoogle Scholar
  10. 10.
    Hobson JA, McCarley RW, Wyzinski PW (1975) Sleep cycle oscillation: reciprocal discharge by two brainstem neuronal groups. Science 189(4196):55–58CrossRefPubMedGoogle Scholar
  11. 11.
    Lin SC, Brown RE, Hussain Shuler MG, Petersen CC, Kepecs A (2015) Optogenetic dissection of the basal forebrain neuromodulatory control of cortical activation, plasticity, and cognition. J Neurosci 35(41):13896–13903CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Saper CB, Fuller PM, Pedersen NP, Lu J, Scammell TE (2010) Sleep state switching. Neuron 68(6):1023–1042CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Jones BE (1993) The organization of central cholinergic systems and their functional importance in sleep-waking states. Prog Brain Res 98:61–71CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Emilia Toth
    • 1
  • Ganne Chaitanya
    • 2
  • Michael Pogwizd
    • 3
  • Diana Pizarro
    • 1
  • Adeel Ilyas
    • 5
  • Steven Pogwizd
    • 4
  • Sandipan Pati
    • 1
  1. 1.Department of NeurologyUniversity of Alabama at BirminghamBirminghamUSA
  2. 2.Department of Clinical NeurosciencesNational Institute of Mental Health and NeurosciencesBangaloreIndia
  3. 3.Department of MathematicsUniversity of Alabama at BirminghamBirminghamUSA
  4. 4.Division of Cardiovascular Diseases, Department of MedicineUniversity of Alabama at BirminghamBirminghamUSA
  5. 5.Department of NeurosurgeryUniversity of Alabama at BirminghamBirminghamUSA

Personalised recommendations