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Breathing Inhibited When Seizures Spread to the Amygdala and upon Amygdala Stimulation
Journal article   Open access   Peer reviewed

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, …
The Journal of neuroscience, Vol.35(28), pp.10281-10289
07/15/2015
DOI: 10.1523/jneurosci.0888-15.2015
PMCID: PMC4502266
PMID: 26180203
url
https://doi.org/10.1523/jneurosci.0888-15.2015View
Published (Version of record) Open Access

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. We took 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. Sudden unexpected death in epilepsy (SUDEP) is the most common cause of death in patients with chronic refractory epilepsy. Impaired breathing during and after seizures is common and suspected to play a role in SUDEP. Understanding the cause of this peri-ictal hypoventilation may lead to preventative strategies. In epilepsy patients, we found that seizure invasion of the amygdala co-occurred with apnea and oxygen desaturation, and electrical stimulation of the amygdala reproduced these respiratory findings. Strikingly, the subjects were unaware of the apnea. These findings indicate a functional connection between the amygdala and brainstem respiratory network in humans and suggest that amygdala seizures may cause loss of spontaneous breathing of which patients are unaware-a combination that could be deadly.
 Apnea - complications Electric Stimulation Humans Evoked Potentials Male Electroencephalography Temporal Lobe - surgery Frontal Lobe - physiology Oxygen - metabolism Epilepsy - complications Magnetic Resonance Imaging Frontal Lobe - surgery Analysis of Variance Image Processing, Computer-Assisted Respiratory Center - pathology Brain Mapping Temporal Lobe - physiology Amygdala - physiology Epilepsy - pathology

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