Amygdala-stimulation-induced apnea is attention and nasal-breathing dependent

William P. Nobis, Stephan Schuele, Jessica W. Templer, Guangyu Zhou, Gregory Lane, Joshua M. Rosenow, Christina Zelano*

*Corresponding author for this work

Research output: Contribution to journalArticle

23 Citations (Scopus)

Abstract

Objective: Evidence suggests that disordered breathing is critically involved in Sudden Unexpected Death in Epilepsy (SUDEP). To that end, evaluating structures that are activated by seizures and can activate brain regions that produce cardiorespiratory changes can further our understanding of the pathophysiology of SUDEP. Past preclinical studies have shown that electrical stimulation of the human amygdala induces apnea, suggesting a role for the amygdala in controlling respiration. In this study, we aimed to both confirm these findings in a larger group of patients with intractable temporal lobe epilepsy (TLE) and also further explore the anatomical and cognitive properties of this effect. Methods: Seven surgical TLE patients had depth electrodes implanted in the amygdala that were used to deliver electrical stimulation during functional mapping preceding resection. Real-time respiratory monitoring was performed in each patient to confirm apnea. Results: Our data confirm that amygdala stimulation reliably induces apnea (occurring in all 7 patients) and further suggest that apnea can be overcome by instructing the patient to inhale, and can be prevented entirely by breathing through the mouth before electrical stimulation. Finally, stimulation-induced apnea occurred only when stimulating the medial-most amygdalar contacts located in the central nucleus. Interpretation: These findings confirm a functional connection between the amygdala and respiratory control in humans. Moreover, they suggest specific amygdalar nuclei may be critical in mediating this effect and that attentional state is critical to apnea mediated by amygdala activation—perhaps alluding to future development of strategies for the prevention of SUDEP. Ann Neurol 2018;83:460–471.

Original languageEnglish (US)
Pages (from-to)460-471
Number of pages12
JournalAnnals of neurology
Volume83
Issue number3
DOIs
StatePublished - Mar 2018

Fingerprint

Apnea
Amygdala
Nose
Respiration
Sudden Death
Electric Stimulation
Epilepsy
Temporal Lobe Epilepsy
Mouth Breathing
Implanted Electrodes
Operative Time
Seizures
Brain

ASJC Scopus subject areas

  • Neurology
  • Clinical Neurology

Cite this

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title = "Amygdala-stimulation-induced apnea is attention and nasal-breathing dependent",
abstract = "Objective: Evidence suggests that disordered breathing is critically involved in Sudden Unexpected Death in Epilepsy (SUDEP). To that end, evaluating structures that are activated by seizures and can activate brain regions that produce cardiorespiratory changes can further our understanding of the pathophysiology of SUDEP. Past preclinical studies have shown that electrical stimulation of the human amygdala induces apnea, suggesting a role for the amygdala in controlling respiration. In this study, we aimed to both confirm these findings in a larger group of patients with intractable temporal lobe epilepsy (TLE) and also further explore the anatomical and cognitive properties of this effect. Methods: Seven surgical TLE patients had depth electrodes implanted in the amygdala that were used to deliver electrical stimulation during functional mapping preceding resection. Real-time respiratory monitoring was performed in each patient to confirm apnea. Results: Our data confirm that amygdala stimulation reliably induces apnea (occurring in all 7 patients) and further suggest that apnea can be overcome by instructing the patient to inhale, and can be prevented entirely by breathing through the mouth before electrical stimulation. Finally, stimulation-induced apnea occurred only when stimulating the medial-most amygdalar contacts located in the central nucleus. Interpretation: These findings confirm a functional connection between the amygdala and respiratory control in humans. Moreover, they suggest specific amygdalar nuclei may be critical in mediating this effect and that attentional state is critical to apnea mediated by amygdala activation—perhaps alluding to future development of strategies for the prevention of SUDEP. Ann Neurol 2018;83:460–471.",
author = "Nobis, {William P.} and Stephan Schuele and Templer, {Jessica W.} and Guangyu Zhou and Gregory Lane and Rosenow, {Joshua M.} and Christina Zelano",
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Amygdala-stimulation-induced apnea is attention and nasal-breathing dependent. / Nobis, William P.; Schuele, Stephan; Templer, Jessica W.; Zhou, Guangyu; Lane, Gregory; Rosenow, Joshua M.; Zelano, Christina.

In: Annals of neurology, Vol. 83, No. 3, 03.2018, p. 460-471.

Research output: Contribution to journalArticle

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AU - Nobis, William P.

AU - Schuele, Stephan

AU - Templer, Jessica W.

AU - Zhou, Guangyu

AU - Lane, Gregory

AU - Rosenow, Joshua M.

AU - Zelano, Christina

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