Acute sleep deprivation enhances susceptibility to the migraine substrate cortical spreading depolarization.

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  • Additional Information
    • Affiliation:
      Neurovascular Research Laboratory, Department of Radiology, Massachusetts General Hospital, Harvard Medical School, Charlestown, MA, USA
      Department of Clinical and Molecular Medicine, Sapienza University of Rome, Rome, Italy
      Department of Neurology, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA, USA
      Department of Pathology, Boston Children's Hospital, Boston, MA, USA
      Stroke Service and Neuroscience Intensive Care Unit, Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA
      Department of Radiology, and Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA
      Department of Radiology, Massachusetts General Hospital, Harvard Medical School, 55 Fruit Street, 02114, Boston, MA, USA
    • Subject Terms:
    • Subject Terms:
    • Abstract:
      Background: Migraine is a common headache disorder, with cortical spreading depolarization (CSD) considered as the underlying electrophysiological event. CSD is a slowly propagating wave of neuronal and glial depolarization. Sleep disorders are well known risk factors for migraine chronification, and changes in wake-sleep pattern such as sleep deprivation are common migraine triggers. The underlying mechanisms are unknown. As a step towards developing an animal model to study this, we test whether sleep deprivation, a modifiable migraine trigger, enhances CSD susceptibility in rodent models. Methods: Acute sleep deprivation was achieved using the "gentle handling method", chosen to minimize stress and avoid confounding bias. Sleep deprivation was started with onset of light (diurnal lighting conditions), and assessment of CSD was performed at the end of a 6 h or 12 h sleep deprivation period. The effect of chronic sleep deprivation on CSD was assessed 6 weeks or 12 weeks after lesioning of the hypothalamic ventrolateral preoptic nucleus. All experiments were done in a blinded fashion with respect to sleep status. During 60 min of continuous topical KCl application, we assessed the total number of CSDs, the direct current shift amplitude and duration of the first CSD, the average and cumulative duration of all CSDs, propagation speed, and electrical CSD threshold. Results: Acute sleep deprivation of 6 h (n = 17) or 12 h (n = 11) duration significantly increased CSD frequency compared to controls (17 ± 4 and 18 ± 2, respectively, vs. 14 ± 2 CSDs/hour in controls; p = 0.003 for both), whereas other electrophysiological properties of CSD were unchanged. Acute total sleep deprivation over 12 h but not over 6 h reduced the electrical threshold of CSD compared to controls (p = 0.037 and p = 0.095, respectively). Chronic partial sleep deprivation in contrast did not affect CSD susceptibility in rats. Conclusions: Acute but not chronic sleep deprivation enhances CSD susceptibility in rodents, possibly underlying its negative impact as a migraine trigger and exacerbating factor. Our findings underscore the importance of CSD as a therapeutic target in migraine and suggest that headache management should identify and treat associated sleep disorders.
    • Journal Subset:
      Biomedical; Continental Europe; Double Blind Peer Reviewed; Editorial Board Reviewed; Europe; Expert Peer Reviewed; Peer Reviewed
    • ISSN:
      1129-2369
    • MEDLINE Info:
      NLM UID: 100940562
    • Publication Date:
      20200709
    • Publication Date:
      20200709
    • DOI:
      10.1186/s10194-020-01155-w
    • Accession Number:
      144404796
  • Citations
    • ABNT:
      NEGRO, A. et al. Acute sleep deprivation enhances susceptibility to the migraine substrate cortical spreading depolarization. Journal of Headache & Pain, [s. l.], v. 21, n. 1, p. 1–11, 2020. DOI 10.1186/s10194-020-01155-w. Disponível em: http://search.ebscohost.com/login.aspx?direct=true&site=eds-live&db=rzh&AN=144404796. Acesso em: 28 set. 2020.
    • AMA:
      Negro A, Seidel JL, Houben T, et al. Acute sleep deprivation enhances susceptibility to the migraine substrate cortical spreading depolarization. Journal of Headache & Pain. 2020;21(1):1-11. doi:10.1186/s10194-020-01155-w
    • APA:
      Negro, A., Seidel, J. L., Houben, T., Yu, E. S., Rosen, I., Arreguin, A. J., Yalcin, N., Shorser-Gentile, L., Pearlman, L., Sadhegian, H., Vetrivelan, R., Chamberlin, N. L., Ayata, C., Martelletti, P., Moskowitz, M. A., & Eikermann-Haerter, K. (2020). Acute sleep deprivation enhances susceptibility to the migraine substrate cortical spreading depolarization. Journal of Headache & Pain, 21(1), 1–11. https://doi.org/10.1186/s10194-020-01155-w
    • Chicago/Turabian: Author-Date:
      Negro, Andrea, Jessica L. Seidel, Thijs Houben, Esther S. Yu, Ike Rosen, Andrea J. Arreguin, Nilufer Yalcin, et al. 2020. “Acute Sleep Deprivation Enhances Susceptibility to the Migraine Substrate Cortical Spreading Depolarization.” Journal of Headache & Pain 21 (1): 1–11. doi:10.1186/s10194-020-01155-w.
    • Harvard:
      Negro, A. et al. (2020) ‘Acute sleep deprivation enhances susceptibility to the migraine substrate cortical spreading depolarization’, Journal of Headache & Pain, 21(1), pp. 1–11. doi: 10.1186/s10194-020-01155-w.
    • Harvard: Australian:
      Negro, A, Seidel, JL, Houben, T, Yu, ES, Rosen, I, Arreguin, AJ, Yalcin, N, Shorser-Gentile, L, Pearlman, L, Sadhegian, H, Vetrivelan, R, Chamberlin, NL, Ayata, C, Martelletti, P, Moskowitz, MA & Eikermann-Haerter, K 2020, ‘Acute sleep deprivation enhances susceptibility to the migraine substrate cortical spreading depolarization’, Journal of Headache & Pain, vol. 21, no. 1, pp. 1–11, viewed 28 September 2020, .
    • MLA:
      Negro, Andrea, et al. “Acute Sleep Deprivation Enhances Susceptibility to the Migraine Substrate Cortical Spreading Depolarization.” Journal of Headache & Pain, vol. 21, no. 1, July 2020, pp. 1–11. EBSCOhost, doi:10.1186/s10194-020-01155-w.
    • Chicago/Turabian: Humanities:
      Negro, Andrea, Jessica L. Seidel, Thijs Houben, Esther S. Yu, Ike Rosen, Andrea J. Arreguin, Nilufer Yalcin, et al. “Acute Sleep Deprivation Enhances Susceptibility to the Migraine Substrate Cortical Spreading Depolarization.” Journal of Headache & Pain 21, no. 1 (July 6, 2020): 1–11. doi:10.1186/s10194-020-01155-w.
    • Vancouver/ICMJE:
      Negro A, Seidel JL, Houben T, Yu ES, Rosen I, Arreguin AJ, et al. Acute sleep deprivation enhances susceptibility to the migraine substrate cortical spreading depolarization. Journal of Headache & Pain [Internet]. 2020 Jul 6 [cited 2020 Sep 28];21(1):1–11. Available from: http://search.ebscohost.com/login.aspx?direct=true&site=eds-live&db=rzh&AN=144404796