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Articles, Neurobiology of Disease

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 and George B. Richerson
Journal of Neuroscience 15 July 2015, 35 (28) 10281-10289; DOI: https://doi.org/10.1523/JNEUROSCI.0888-15.2015
Brian J. Dlouhy
1Departments of Neurosurgery,
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Brian K. Gehlbach
2Internal Medicine,
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Collin J. Kreple
3Psychiatry,
4Medical Scientist Training Program,
5Molecular Physiology and Biophysics,
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Hiroto Kawasaki
1Departments of Neurosurgery,
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Hiroyuki Oya
1Departments of Neurosurgery,
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Colin Buzza
3Psychiatry,
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Mark A. Granner
6Neurology, and
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Michael J. Welsh
2Internal Medicine,
5Molecular Physiology and Biophysics,
7Interdisciplinary Graduate Program in Neuroscience, University of Iowa, Iowa City, Iowa 52242,
8Howard Hughes Medical Institute, Chevy Chase, Maryland 20815, and
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Matthew A. Howard
1Departments of Neurosurgery,
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John A. Wemmie
1Departments of Neurosurgery,
2Internal Medicine,
3Psychiatry,
5Molecular Physiology and Biophysics,
7Interdisciplinary Graduate Program in Neuroscience, University of Iowa, Iowa City, Iowa 52242,
9Department of Veterans Affairs Medical Center, Iowa City, Iowa 52242
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George B. Richerson
5Molecular Physiology and Biophysics,
6Neurology, and
7Interdisciplinary Graduate Program in Neuroscience, University of Iowa, Iowa City, Iowa 52242,
9Department of Veterans Affairs Medical Center, Iowa City, Iowa 52242
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    Figure 1.

    Central apnea occurred when seizures spread to the left amygdala. A, Intraoperative photographs of J.K.'s frontotemporal lobe before (left) and after (right) placement of intracranial electrodes. F, frontal lobe; T, temporal lobe. Sylvian fissure is indicated by a dashed line. B, Surface-rendered MR images of J.K.'s brain showing the location of each surface electrode contact (circles). C, Axial MR images showing the location of the right amygdala depth electrode contact and left amygdala depth electrode contacts (arrow, most medial contact). D, Anatomic diagram of J.K.'s right and left temporal lobe showing amygdala subnuclei with superimposed amygdala depth electrode contacts (gray circles). Lateral nucleus, red; basolateral nucleus, yellow; basomedial nucleus, magenta; central nucleus, blue; hippocampus, green. E, EEG of complex partial seizure with onset in the right subfrontal cortex (red circles in B). Breathing pattern was normal before and after seizure initiation. Apnea coincided with seizure spread to the left amygdala (gray circles in D) and before seizure spread to the right amygdala, right temporal pole (green circles in B), right medial frontal cortex (yellow circles in B), and right posterior frontal cortex (orange circles in B).

  • Figure 2.
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    Figure 2.

    Electrical stimulation of the amygdala reproduced central apnea and oxygen desaturation. A, Anatomic scaled line diagram of J.K.'s left temporal lobe showing the locations of amygdala depth electrode contacts (gray circles) within the basolateral (yellow) and lateral nuclei (red) of the amygdala. Stimulating the left basolateral and lateral amygdala caused apnea (B), slight slowing of the heart rate, and decreased oxygen saturation (SpO2; C). D, Anatomic diagram of J.K.'s right temporal lobe showing amygdala subnuclei with superimposed amygdala depth electrode contact (gray circle) in the basolateral (yellow) and lateral nuclei (red). Stimulating the right amygdala caused apnea (E), slight slowing of the heart rate, and reduced oxygen saturation (SpO2; F). G, Average respiratory rate (H) and oxygen saturation at baseline and during 20–30 s electrical stimulation trials (nonamygdala stimulation, n = 3; left amygdala stimulation, n = 6; right amygdala stimulation, n = 3). ****p < 0.0001; two-way ANOVA with Bonferroni post hoc test. Error bars indicate SEM. The oxygen desaturation peaked after amygdala stimulation because oxygen saturation was measured by a pulse oximeter on the extremities resulting in a 20 s delay.

  • Figure 3.
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    Figure 3.

    J.K. lacked dyspnea and awareness of amygdala stimulation-evoked apnea. J.K. was completely unaware of and displayed no dyspnea with 48 s of apnea evoked by a 47 s stimulation of the left amygdala (A), which resulted in oxygen desaturation to 87% (B). C, J.K. voluntarily held his breath for 60 s, which caused an oxygen desaturation to 91% and severe shortness of breath and dyspnea (D). E, J.K. was agnostic to repeated amygdala stimulation (5 s on and off), which first caused sustained apnea, followed by a new respiratory pattern consisting of two breaths during the 5 s without stimulation and apnea during the period of stimulation. F, Breathing during a 5 s on and 5 s off amygdala stimulation paradigm over a period of 5 min resulted in initiated breaths during the 5 s off stimulation and apnea during the periods of stimulation and resulted in a new intermittent breathing pattern. This lasted the entire period of the stimulation paradigm. J.K. was unaware of any breathing changes during this stimulation.

  • Figure 4.
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    Figure 4.

    Apnea did not occur while speaking during amygdala stimulation and it did not occur during stimulation outside and lateral to the amygdala. A, Anatomic diagram of J.K.'s left temporal lobe showed amygdala subnuclei with superimposed amygdala depth electrode contacts (gray circles) in the basolateral (yellow) and lateral nuclei (red). B, C, Stimulating these contacts while speaking did not result in apnea and oxygen saturation (SpO2) remained unchanged, D, Anatomic diagram of J.K.'s right temporal lobe showing amygdala subnuclei with superimposed locations of depth electrode contacts (gray circles) immediately lateral to the amygdala. Stimulating these contacts just lateral and outside the amygdala did not cause changes in breathing (E) or oxygen saturation (SpO2; F). The nonspecific change in the plethysmography tracing immediately after stimulation (E) was associated with the patient's movement and when the patient stopped moving, the tracing returned to baseline.

  • Figure 5.
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    Figure 5.

    The respiratory effects of amygdala stimulation were reproduced in two other subjects (K.D. and S.P.). A, Anatomic diagram of K.D.'s right temporal lobe showing amygdala subnuclei with superimposed amygdala depth electrode contacts (gray circles) in the basolateral and lateral nuclei. Lateral nucleus, red; basolateral nucleus, yellow. B, Stimulating the right amygdala caused apnea and a slight slowing of the heart rate. C, Average respiratory rate at baseline, during electrical stimulation trials (20–30 s) and the 10–20 s after stimulation (n = 6). D, Schematic depiction of the location of intraoperative amygdala electrical stimulation performed using a handheld device in subject S.P. E, Average respiratory rate at baseline, during intraoperative bipolar electrical stimulation (10 s), and after stimulation (n = 3). ****p < 0.0001; **p < 0.05; one-way ANOVA with Bonferroni post hoc test. Error bars indicate SEM.

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The Journal of Neuroscience: 35 (28)
Journal of Neuroscience
Vol. 35, Issue 28
15 Jul 2015
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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
Journal of Neuroscience 15 July 2015, 35 (28) 10281-10289; DOI: 10.1523/JNEUROSCI.0888-15.2015

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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
Journal of Neuroscience 15 July 2015, 35 (28) 10281-10289; DOI: 10.1523/JNEUROSCI.0888-15.2015
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Keywords

  • amygdala
  • brainstem
  • breathing
  • epilepsy
  • sudden death
  • SUDEP

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