Breathing inhibited when seizures spread to the amygdala and upon amygdala stimulation

Brian J. Dlouhy, Brian K. Gehlbach, Collin J. Kreple, Hiroto Kawasaki, Hiroyuki Oya, Colin Buzza, Mark A. Granner, Michael J. Welsh, Matthew A. Howard, John A. Wemmie, George B. Richerson

Research output: Contribution to journalArticlepeer-review

178 Scopus citations

Abstract

Sudden unexpected death in epilepsy (SUDEP) is increasingly recognized as a common and devastating problem. Because impaired breathing is thought to play a critical role in these deaths, we sought to identify forebrain sites underlying seizure-evoked hypoventilation in humans.Wetook advantage of an extraordinary clinical opportunity to study a research participant with medically intractable epilepsy who had extensive bilateral frontotemporal electrode coverage while breathing was monitored during seizures recorded by intracranial electrodes and mapped by high-resolution brain imaging. We found that central apnea and O2 desaturation occurred when seizures spread to the amygdala. In the same patient, localized electrical stimulation of the amygdala reproduced the apnea and O2 desaturation. Similar effects of amygdala stimulation were observed in two additional subjects, including one without a seizure disorder. The participants were completely unaware of the apnea evoked by stimulation and expressed no dyspnea, despite being awake and vigilant. In contrast, voluntary breath holding of similar duration caused severe dyspnea. These findings suggest a functional connection between the amygdala and medullary respiratory network in humans. Moreover, they suggest that seizure spread to the amygdala may cause loss of spontaneous breathing of which patients are unaware, and thus has potential to contribute to SUDEP.

Original languageEnglish
Pages (from-to)10281-10289
Number of pages9
JournalJournal of Neuroscience
Volume35
Issue number28
DOIs
StatePublished - Jul 15 2015

Keywords

  • Amygdala
  • Brainstem
  • Breathing
  • Epilepsy
  • SUDEP
  • Sudden death

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