Neurophysiologic effects of transcutaneous auricular vagus nerve stimulation (taVNS) via electrical stimulation of the tragus: A concurrent taVNS/fMRI study and review

Electrical stimulation of the auricular branch of the vagus nerve (ABVN) via transcutaneous auricular vagus nerve stimulation (taVNS) may influence afferent vagal networks. There have been 5 prior taVNS/fMRI studies, with inconsistent findings due to variability in stimulation targets and parameters...

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Published in:Brain stimulation Vol. 11; no. 3; pp. 492 - 500
Main Authors: Badran, Bashar W., Dowdle, Logan T., Mithoefer, Oliver J., LaBate, Nicholas T., Coatsworth, James, Brown, Joshua C., DeVries, William H., Austelle, Christopher W., McTeague, Lisa M., George, Mark S.
Format: Journal Article
Language:English
Published: United States Elsevier Inc 01.05.2018
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ISSN:1935-861X, 1876-4754, 1876-4754
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Abstract Electrical stimulation of the auricular branch of the vagus nerve (ABVN) via transcutaneous auricular vagus nerve stimulation (taVNS) may influence afferent vagal networks. There have been 5 prior taVNS/fMRI studies, with inconsistent findings due to variability in stimulation targets and parameters. We developed a taVNS/fMRI system to enable concurrent electrical stimulation and fMRI acquisition to compare the effects of taVNS in relation to control stimulation. We enrolled 17 healthy adults in this single-blind, crossover taVNS/fMRI trial. Based on parameters shown to affect heart rate in healthy volunteers, participants received either left tragus (active) or earlobe (control) stimulation at 500 μs 25 HZ for 60 s (repeated 3 times over 6 min). Whole brain fMRI analysis was performed exploring the effect of: active stimulation, control stimulation, and the comparison. Region of interest analysis of the midbrain and brainstem was also conducted. Active stimulation produced significant increased BOLD signal in the contralateral postcentral gyrus, bilateral insula, frontal cortex, right operculum, and left cerebellum. Control stimulation produced BOLD signal activation in the contralateral postcentral gyrus. In the active vs. control contrast, tragus stimulation produced significantly greater BOLD increases in the right caudate, bilateral anterior cingulate, cerebellum, left prefrontal cortex, and mid-cingulate. Stimulation of the tragus activates the cerebral afferents of the vagal pathway and combined with our review of the literature suggest that taVNS is a promising form of VNS. Future taVNS/fMRI studies should systematically explore various parameters and alternative stimulation targets aimed to optimize this novel form of neuromodulation. •A taVNS/fMRI system was developed to explore brain effects of stimulation.•Tragus stimulation reliably activates cerebral afferent vagal networks.•Earlobe stimulation demonstrates solely somatosensory activation.•Bilateral ACC and frontal activation is produced by 60s active stimulation.•taVNS at 500 μs 25 Hz may be a biologically active stimulation parameter.
AbstractList Electrical stimulation of the auricular branch of the vagus nerve (ABVN) via transcutaneous auricular vagus nerve stimulation (taVNS) may influence afferent vagal networks. There have been 5 prior taVNS/fMRI studies, with inconsistent findings due to variability in stimulation targets and parameters.BACKGROUNDElectrical stimulation of the auricular branch of the vagus nerve (ABVN) via transcutaneous auricular vagus nerve stimulation (taVNS) may influence afferent vagal networks. There have been 5 prior taVNS/fMRI studies, with inconsistent findings due to variability in stimulation targets and parameters.We developed a taVNS/fMRI system to enable concurrent electrical stimulation and fMRI acquisition to compare the effects of taVNS in relation to control stimulation.OBJECTIVEWe developed a taVNS/fMRI system to enable concurrent electrical stimulation and fMRI acquisition to compare the effects of taVNS in relation to control stimulation.We enrolled 17 healthy adults in this single-blind, crossover taVNS/fMRI trial. Based on parameters shown to affect heart rate in healthy volunteers, participants received either left tragus (active) or earlobe (control) stimulation at 500 μs 25 HZ for 60 s (repeated 3 times over 6 min). Whole brain fMRI analysis was performed exploring the effect of: active stimulation, control stimulation, and the comparison. Region of interest analysis of the midbrain and brainstem was also conducted.METHODSWe enrolled 17 healthy adults in this single-blind, crossover taVNS/fMRI trial. Based on parameters shown to affect heart rate in healthy volunteers, participants received either left tragus (active) or earlobe (control) stimulation at 500 μs 25 HZ for 60 s (repeated 3 times over 6 min). Whole brain fMRI analysis was performed exploring the effect of: active stimulation, control stimulation, and the comparison. Region of interest analysis of the midbrain and brainstem was also conducted.Active stimulation produced significant increased BOLD signal in the contralateral postcentral gyrus, bilateral insula, frontal cortex, right operculum, and left cerebellum. Control stimulation produced BOLD signal activation in the contralateral postcentral gyrus. In the active vs. control contrast, tragus stimulation produced significantly greater BOLD increases in the right caudate, bilateral anterior cingulate, cerebellum, left prefrontal cortex, and mid-cingulate.RESULTSActive stimulation produced significant increased BOLD signal in the contralateral postcentral gyrus, bilateral insula, frontal cortex, right operculum, and left cerebellum. Control stimulation produced BOLD signal activation in the contralateral postcentral gyrus. In the active vs. control contrast, tragus stimulation produced significantly greater BOLD increases in the right caudate, bilateral anterior cingulate, cerebellum, left prefrontal cortex, and mid-cingulate.Stimulation of the tragus activates the cerebral afferents of the vagal pathway and combined with our review of the literature suggest that taVNS is a promising form of VNS. Future taVNS/fMRI studies should systematically explore various parameters and alternative stimulation targets aimed to optimize this novel form of neuromodulation.CONCLUSIONStimulation of the tragus activates the cerebral afferents of the vagal pathway and combined with our review of the literature suggest that taVNS is a promising form of VNS. Future taVNS/fMRI studies should systematically explore various parameters and alternative stimulation targets aimed to optimize this novel form of neuromodulation.
Electrical stimulation of the auricular branch of the vagus nerve (ABVN) via transcutaneous auricular vagus nerve stimulation (taVNS) may influence afferent vagal networks. There have been 5 prior taVNS/fMRI studies, with inconsistent findings due to variability in stimulation targets and parameters. We developed a taVNS/fMRI system to enable concurrent electrical stimulation and fMRI acquisition to compare the effects of taVNS in relation to control stimulation. We enrolled 17 healthy adults in this single-blind, crossover taVNS/fMRI trial. Based on parameters shown to affect heart rate in healthy volunteers, participants received either left tragus (active) or earlobe (control) stimulation at 500 μs 25 HZ for 60 s (repeated 3 times over 6 min). Whole brain fMRI analysis was performed exploring the effect of: active stimulation, control stimulation, and the comparison. Region of interest analysis of the midbrain and brainstem was also conducted. Active stimulation produced significant increased BOLD signal in the contralateral postcentral gyrus, bilateral insula, frontal cortex, right operculum, and left cerebellum. Control stimulation produced BOLD signal activation in the contralateral postcentral gyrus. In the active vs. control contrast, tragus stimulation produced significantly greater BOLD increases in the right caudate, bilateral anterior cingulate, cerebellum, left prefrontal cortex, and mid-cingulate. Stimulation of the tragus activates the cerebral afferents of the vagal pathway and combined with our review of the literature suggest that taVNS is a promising form of VNS. Future taVNS/fMRI studies should systematically explore various parameters and alternative stimulation targets aimed to optimize this novel form of neuromodulation. •A taVNS/fMRI system was developed to explore brain effects of stimulation.•Tragus stimulation reliably activates cerebral afferent vagal networks.•Earlobe stimulation demonstrates solely somatosensory activation.•Bilateral ACC and frontal activation is produced by 60s active stimulation.•taVNS at 500 μs 25 Hz may be a biologically active stimulation parameter.
Electrical stimulation of the auricular branch of the vagus nerve (ABVN) via transcutaneous auricular vagus nerve stimulation (taVNS) may influence afferent vagal networks. There have been 5 prior taVNS/fMRI studies, with inconsistent findings due to variability in stimulation targets and parameters. We developed a taVNS/fMRI system to enable concurrent electrical stimulation and fMRI acquisition to compare the effects of taVNS in relation to control stimulation. We enrolled 17 healthy adults in this single-blind, crossover taVNS/fMRI trial. Based on parameters shown to affect heart rate in healthy volunteers, participants received either left tragus (active) or earlobe (control) stimulation at 500 μs 25 HZ for 60 s (repeated 3 times over 6 min). Whole brain fMRI analysis was performed exploring the effect of: active stimulation, control stimulation, and the comparison. Region of interest analysis of the midbrain and brainstem was also conducted. Active stimulation produced significant increased BOLD signal in the contralateral postcentral gyrus, bilateral insula, frontal cortex, right operculum, and left cerebellum. Control stimulation produced BOLD signal activation in the contralateral postcentral gyrus. In the active vs. control contrast, tragus stimulation produced significantly greater BOLD increases in the right caudate, bilateral anterior cingulate, cerebellum, left prefrontal cortex, and mid-cingulate. Stimulation of the tragus activates the cerebral afferents of the vagal pathway and combined with our review of the literature suggest that taVNS is a promising form of VNS. Future taVNS/fMRI studies should systematically explore various parameters and alternative stimulation targets aimed to optimize this novel form of neuromodulation.
Author George, Mark S.
Dowdle, Logan T.
Badran, Bashar W.
Mithoefer, Oliver J.
Coatsworth, James
Brown, Joshua C.
McTeague, Lisa M.
DeVries, William H.
Austelle, Christopher W.
LaBate, Nicholas T.
AuthorAffiliation a Department of Neuroscience, Medical University of South Carolina, Charleston, SC, 29425, United States
c Department of Psychology, University of New Mexico, Albuquerque, NM, 87131, United States
d US Army Research Lab, Aberdeen Proving Ground, MD, 21005, United States
g Department of Neurology, Medical University of South Carolina, Charleston, SC, 29425, United States
b Department of Psychiatry, Medical University of South Carolina, Charleston, SC, 29425, United States
h Ralph H. Johnson VA Medical Center, Charleston, SC, 29401, United States
e College of Charleston, Charleston, SC, 29403, United States
f Center for Biomedical Imaging, Medical University of South Carolina, Charleston, SC, 29425, United States
AuthorAffiliation_xml – name: a Department of Neuroscience, Medical University of South Carolina, Charleston, SC, 29425, United States
– name: g Department of Neurology, Medical University of South Carolina, Charleston, SC, 29425, United States
– name: b Department of Psychiatry, Medical University of South Carolina, Charleston, SC, 29425, United States
– name: e College of Charleston, Charleston, SC, 29403, United States
– name: f Center for Biomedical Imaging, Medical University of South Carolina, Charleston, SC, 29425, United States
– name: c Department of Psychology, University of New Mexico, Albuquerque, NM, 87131, United States
– name: d US Army Research Lab, Aberdeen Proving Ground, MD, 21005, United States
– name: h Ralph H. Johnson VA Medical Center, Charleston, SC, 29401, United States
Author_xml – sequence: 1
  givenname: Bashar W.
  surname: Badran
  fullname: Badran, Bashar W.
  email: badran@musc.edu
  organization: Department of Neuroscience, Medical University of South Carolina, Charleston, SC, 29425, United States
– sequence: 2
  givenname: Logan T.
  surname: Dowdle
  fullname: Dowdle, Logan T.
  organization: Department of Neuroscience, Medical University of South Carolina, Charleston, SC, 29425, United States
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  givenname: Oliver J.
  surname: Mithoefer
  fullname: Mithoefer, Oliver J.
  organization: Department of Psychiatry, Medical University of South Carolina, Charleston, SC, 29425, United States
– sequence: 4
  givenname: Nicholas T.
  surname: LaBate
  fullname: LaBate, Nicholas T.
  organization: College of Charleston, Charleston, SC, 29403, United States
– sequence: 5
  givenname: James
  surname: Coatsworth
  fullname: Coatsworth, James
  organization: Center for Biomedical Imaging, Medical University of South Carolina, Charleston, SC, 29425, United States
– sequence: 6
  givenname: Joshua C.
  surname: Brown
  fullname: Brown, Joshua C.
  organization: Department of Psychiatry, Medical University of South Carolina, Charleston, SC, 29425, United States
– sequence: 7
  givenname: William H.
  surname: DeVries
  fullname: DeVries, William H.
  organization: Department of Psychiatry, Medical University of South Carolina, Charleston, SC, 29425, United States
– sequence: 8
  givenname: Christopher W.
  surname: Austelle
  fullname: Austelle, Christopher W.
  organization: Department of Psychiatry, Medical University of South Carolina, Charleston, SC, 29425, United States
– sequence: 9
  givenname: Lisa M.
  surname: McTeague
  fullname: McTeague, Lisa M.
  organization: Department of Psychiatry, Medical University of South Carolina, Charleston, SC, 29425, United States
– sequence: 10
  givenname: Mark S.
  surname: George
  fullname: George, Mark S.
  organization: Department of Neuroscience, Medical University of South Carolina, Charleston, SC, 29425, United States
BackLink https://www.ncbi.nlm.nih.gov/pubmed/29361441$$D View this record in MEDLINE/PubMed
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Keywords fMRI
Anterior cingulate cortex (ACC)
Ear stimulation
Transcutaneous auricular vagus nerve stimulation (taVNS)
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Snippet Electrical stimulation of the auricular branch of the vagus nerve (ABVN) via transcutaneous auricular vagus nerve stimulation (taVNS) may influence afferent...
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StartPage 492
SubjectTerms Adolescent
Adult
Anterior cingulate cortex (ACC)
Brain - physiology
Cross-Over Studies
Ear stimulation
Female
fMRI
Functional Neuroimaging
Healthy Volunteers
Humans
Magnetic Resonance Imaging - methods
Male
Middle Aged
Single-Blind Method
Transcutaneous auricular vagus nerve stimulation (taVNS)
Transcutaneous Electric Nerve Stimulation - methods
Vagus Nerve - physiology
Vagus Nerve Stimulation - methods
Young Adult
Title Neurophysiologic effects of transcutaneous auricular vagus nerve stimulation (taVNS) via electrical stimulation of the tragus: A concurrent taVNS/fMRI study and review
URI https://www.clinicalkey.com/#!/content/1-s2.0-S1935861X17310252
https://dx.doi.org/10.1016/j.brs.2017.12.009
https://www.ncbi.nlm.nih.gov/pubmed/29361441
https://www.proquest.com/docview/1990851690
https://pubmed.ncbi.nlm.nih.gov/PMC6487660
Volume 11
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