Literature DB >> 32163374

A human amygdala site that inhibits respiration and elicits apnea in pediatric epilepsy.

Ariane E Rhone1,2, Christopher K Kovach1,2, Gail Is Harmata1,2,3,4,5,6, Alyssa W Sullivan7, Daniel Tranel2,7,8, Michael A Ciliberto9, Matthew A Howard1,2,3, George B Richerson2,3,4,8,10, Mitchell Steinschneider11, John A Wemmie1,2,3,4,6,8,10,12, Brian J Dlouhy1,2,3.   

Abstract

BACKGROUNDSeizure-induced inhibition of respiration plays a critical role in sudden unexpected death in epilepsy (SUDEP). However, the mechanisms underlying seizure-induced central apnea in pediatric epilepsy are unknown.METHODSWe studied 8 pediatric patients with intractable epilepsy undergoing intracranial electroencephalography. We recorded respiration during seizures and during electrical stimulation mapping of 174 forebrain sites. A machine-learning algorithm was used to delineate brain regions that inhibit respiration.RESULTSIn 2 patients, apnea coincided with seizure spread to the amygdala. Supporting a role for the amygdala in breathing inhibition in children, electrically stimulating the amygdala produced apnea in all 8 subjects (3-17 years old). These effects did not depend on epilepsy type and were relatively specific to the amygdala, as no other site affected breathing. Remarkably, patients were unaware that they had stopped breathing, and none reported dyspnea or arousal, findings critical for SUDEP. Finally, a machine-learning algorithm based on 45 stimulation sites and 210 stimulation trials identified a focal subregion in the human amygdala that consistently produced apnea. This site, which we refer to as the amygdala inhibition of respiration (AIR) site includes the medial subregion of the basal nuclei, cortical and medial nuclei, amygdala transition areas, and intercalated neurons.CONCLUSIONSA focal site in the amygdala inhibits respiration and induces apnea (AIR site) when electrically stimulated and during seizures in children with epilepsy. This site may prove valuable for determining those at greatest risk for SUDEP and as a therapeutic target.FUNDINGNational Institute of Neurological Disorders and Stroke - Congress of Neurological Surgeons, National Institute of General Medical Sciences, Roy J. Carver Charitable Trust.

Entities:  

Keywords:  Neurological disorders; Neuroscience; Respiration; Seizures

Mesh:

Year:  2020        PMID: 32163374      PMCID: PMC7213805          DOI: 10.1172/jci.insight.134852

Source DB:  PubMed          Journal:  JCI Insight        ISSN: 2379-3708


  64 in total

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Authors:  B R KAADA; H JASPER
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2.  Amygdala and hippocampus are symptomatogenic zones for central apneic seizures.

Authors:  Nuria Lacuey; Bilal Zonjy; Luisa Londono; Samden D Lhatoo
Journal:  Neurology       Date:  2017-01-13       Impact factor: 9.910

3.  Processing of facial emotion in the human fusiform gyrus.

Authors:  Hiroto Kawasaki; Naotsugu Tsuchiya; Christopher K Kovach; Kirill V Nourski; Hiroyuki Oya; Matthew A Howard; Ralph Adolphs
Journal:  J Cogn Neurosci       Date:  2011-12-20       Impact factor: 3.225

4.  Long-term mortality in childhood-onset epilepsy.

Authors:  Matti Sillanpää; Shlomo Shinnar
Journal:  N Engl J Med       Date:  2010-12-23       Impact factor: 91.245

Review 5.  The serotonin axis: Shared mechanisms in seizures, depression, and SUDEP.

Authors:  George B Richerson; Gordon F Buchanan
Journal:  Epilepsia       Date:  2011-01       Impact factor: 5.864

6.  Brain responses associated with consciousness of breathlessness (air hunger).

Authors:  M Liotti; S Brannan; G Egan; R Shade; L Madden; B Abplanalp; R Robillard; J Lancaster; F E Zamarripa; P T Fox; D Denton
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7.  Amygdaloid projections to the mesencephalon, pons and medulla oblongata in the cat.

Authors:  D A Hopkins; G Holstege
Journal:  Exp Brain Res       Date:  1978-08-15       Impact factor: 1.972

8.  Impaired and facilitated functional networks in temporal lobe epilepsy.

Authors:  Luigi Maccotta; Biyu J He; Abraham Z Snyder; Lawrence N Eisenman; Tammie L Benzinger; Beau M Ances; Maurizio Corbetta; R Edward Hogan
Journal:  Neuroimage Clin       Date:  2013-06-25       Impact factor: 4.881

9.  Age-Related Structural Alterations in Human Amygdala Networks: Reflections on Correlations Between White Matter Structure and Effective Connectivity.

Authors:  Yuhao Jiang; Yin Tian; Zhongyan Wang
Journal:  Front Hum Neurosci       Date:  2019-07-05       Impact factor: 3.169

10.  SUDEP in the North American SUDEP Registry: The full spectrum of epilepsies.

Authors:  Chloe Verducci; Fizza Hussain; Elizabeth Donner; Brian D Moseley; Jeffrey Buchhalter; Dale Hesdorffer; Daniel Friedman; Orrin Devinsky
Journal:  Neurology       Date:  2019-06-19       Impact factor: 9.910

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  11 in total

Review 1.  Review: Neuropathology findings in autonomic brain regions in SUDEP and future research directions.

Authors:  Smriti Patodia; Alyma Somani; Maria Thom
Journal:  Auton Neurosci       Date:  2021-07-31       Impact factor: 3.145

2.  Disruption of Synaptic Transmission in the Bed Nucleus of the Stria Terminalis Reduces Seizure-Induced Death in DBA/1 Mice and Alters Brainstem E/I Balance.

Authors:  Maya Xia; Benjamin Owen; Jeremy Chiang; Alyssa Levitt; Katherine Preisinger; Wen Wei Yan; Ragan Huffman; William P Nobis
Journal:  ASN Neuro       Date:  2022 Jan-Dec       Impact factor: 5.200

3.  Limbic and paralimbic respiratory modulation: From inhibition to enhancement.

Authors:  Ganne Chaitanya; Johnson P Hampson; Emilia Toth; Norma J Hupp; Jaison S Hampson; John C Mosher; Sandipan Pati; Samden D Lhatoo; Nuria Lacuey
Journal:  Epilepsia       Date:  2022-05-19       Impact factor: 6.740

4.  Electrical Stimulation-Induced Seizures and Breathing Dysfunction: A Systematic Review of New Insights Into the Epileptogenic and Symptomatogenic Zones.

Authors:  Manuela Ochoa-Urrea; Mojtaba Dayyani; Behnam Sadeghirad; Nitin Tandon; Nuria Lacuey; Samden D Lhatoo
Journal:  Front Hum Neurosci       Date:  2021-01-22       Impact factor: 3.169

5.  Serotonin transporter in the temporal lobe, hippocampus and amygdala in SUDEP.

Authors:  Smriti Patodia; Alyma Somani; Joan Liu; Alice Cattaneo; Beatrice Paradiso; Maria Garcia; Muhammad Othman; Beate Diehl; Orrin Devinsky; James D Mills; Jackie Foong; Maria Thom
Journal:  Brain Pathol       Date:  2022-04-27       Impact factor: 7.611

Review 6.  The role of sleep state and time of day in modulating breathing in epilepsy: implications for sudden unexpected death in epilepsy.

Authors:  Katelyn G Joyal; Benjamin L Kreitlow; Gordon F Buchanan
Journal:  Front Neural Circuits       Date:  2022-08-23       Impact factor: 3.342

7.  Regional variation in brain tissue texture in patients with tonic-clonic seizures.

Authors:  Jennifer A Ogren; Luke A Allen; Bhaswati Roy; Beate Diehl; John M Stern; Dawn S Eliashiv; Samden D Lhatoo; Ronald M Harper; Rajesh Kumar
Journal:  PLoS One       Date:  2022-09-22       Impact factor: 3.752

8.  Forebrain epileptiform activity is not required for seizure-induced apnea in a mouse model of Scn8a epilepsy.

Authors:  Ian C Wenker; Alexis R Boscia; Christine Lewis; Anas Tariq; Raquel Miralles; Jessica C Hanflink; Priyanka Saraf; Manoj K Patel
Journal:  Front Neural Circuits       Date:  2022-09-07       Impact factor: 3.342

9.  Mapping effective connectivity of human amygdala subdivisions with intracranial stimulation.

Authors:  Masahiro Sawada; Ralph Adolphs; Brian J Dlouhy; Rick L Jenison; Ariane E Rhone; Christopher K Kovach; Jeremy D W Greenlee; Matthew A Howard Iii; Hiroyuki Oya
Journal:  Nat Commun       Date:  2022-08-20       Impact factor: 17.694

10.  Human Primary Olfactory Amygdala Subregions Form Distinct Functional Networks, Suggesting Distinct Olfactory Functions.

Authors:  Torben Noto; Guangyu Zhou; Qiaohan Yang; Gregory Lane; Christina Zelano
Journal:  Front Syst Neurosci       Date:  2021-12-09
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