Stimulus frequency modulates brainstem response to respiratory-gated transcutaneous auricular vagus nerve stimulation.


Journal

Brain stimulation
ISSN: 1876-4754
Titre abrégé: Brain Stimul
Pays: United States
ID NLM: 101465726

Informations de publication

Date de publication:
Historique:
received: 01 11 2019
revised: 22 01 2020
accepted: 18 03 2020
pubmed: 8 5 2020
medline: 15 12 2020
entrez: 8 5 2020
Statut: ppublish

Résumé

The therapeutic potential of transcutaneous auricular VNS (taVNS) is currently being explored for numerous clinical applications. However, optimized response for different clinical indications may depend on specific neuromodulation parameters, and systematic assessments of their influence are still needed to optimize this promising approach. We proposed that stimulation frequency would have a significant effect on nucleus tractus solitarii (NTS) functional MRI (fMRI) response to respiratory-gated taVNS (RAVANS). Brainstem fMRI response to auricular RAVANS (cymba conchae) was assessed for four different stimulation frequencies (2, 10, 25, 100 Hz). Sham (no current) stimulation was used to control for respiration effects on fMRI signal. Our findings demonstrated that RAVANS delivered at 100 Hz evoked the strongest brainstem response, localized to a cluster in the left (ipsilateral) medulla and consistent with purported NTS. A co-localized, although weaker, response was found for 2 Hz RAVANS. Furthermore, RAVANS delivered at 100 Hz also evoked stronger fMRI responses for important monoamine neurotransmitter source nuclei (LC, noradrenergic; MR, DR, serotonergic) and pain/homeostatic regulation nuclei (i.e. PAG). Our fMRI results support previous localization of taVNS afference to pontomedullary aspect of NTS in the human brainstem, and demonstrate the significant influence of the stimulation frequency on brainstem fMRI response.

Sections du résumé

BACKGROUND
The therapeutic potential of transcutaneous auricular VNS (taVNS) is currently being explored for numerous clinical applications. However, optimized response for different clinical indications may depend on specific neuromodulation parameters, and systematic assessments of their influence are still needed to optimize this promising approach.
HYPOTHESIS
We proposed that stimulation frequency would have a significant effect on nucleus tractus solitarii (NTS) functional MRI (fMRI) response to respiratory-gated taVNS (RAVANS).
METHODS
Brainstem fMRI response to auricular RAVANS (cymba conchae) was assessed for four different stimulation frequencies (2, 10, 25, 100 Hz). Sham (no current) stimulation was used to control for respiration effects on fMRI signal.
RESULTS
Our findings demonstrated that RAVANS delivered at 100 Hz evoked the strongest brainstem response, localized to a cluster in the left (ipsilateral) medulla and consistent with purported NTS. A co-localized, although weaker, response was found for 2 Hz RAVANS. Furthermore, RAVANS delivered at 100 Hz also evoked stronger fMRI responses for important monoamine neurotransmitter source nuclei (LC, noradrenergic; MR, DR, serotonergic) and pain/homeostatic regulation nuclei (i.e. PAG).
CONCLUSION
Our fMRI results support previous localization of taVNS afference to pontomedullary aspect of NTS in the human brainstem, and demonstrate the significant influence of the stimulation frequency on brainstem fMRI response.

Identifiants

pubmed: 32380448
pii: S1935-861X(20)30064-4
doi: 10.1016/j.brs.2020.03.011
pmc: PMC7931850
mid: NIHMS1580167
pii:
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

970-978

Subventions

Organisme : NIAMS NIH HHS
ID : R01 AR064367
Pays : United States
Organisme : NIDDK NIH HHS
ID : R21 DK116029
Pays : United States
Organisme : NCCIH NIH HHS
ID : P01 AT009965
Pays : United States
Organisme : NCCIH NIH HHS
ID : R33 AT009306
Pays : United States
Organisme : NIBIB NIH HHS
ID : P41 EB015896
Pays : United States
Organisme : NIH HHS
ID : OT2 OD023867
Pays : United States
Organisme : NCCIH NIH HHS
ID : R01 AT007550
Pays : United States
Organisme : NCCIH NIH HHS
ID : P01 AT006663
Pays : United States
Organisme : NCRR NIH HHS
ID : S10 RR023043
Pays : United States
Organisme : NCCIH NIH HHS
ID : R61 AT009306
Pays : United States

Informations de copyright

Copyright © 2020 The Author(s). Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of competing interest VN and JG have a financial interest in Cala Health which is licensing the RAVANS technology from MGH. These investigators’ interests were reviewed and are managed by the Massachusetts General Hospital and Partners HealthCare in accordance with their institutional policies.

Références

BMC Complement Altern Med. 2012 Dec 14;12:255
pubmed: 23241431
Neuroimage. 2011 Jan 1;54(1):313-27
pubmed: 20656036
J Stroke Cerebrovasc Dis. 2018 Jul;27(7):1998-2005
pubmed: 29580658
Auton Neurosci. 2008 Feb 29;138(1-2):50-6
pubmed: 18068545
Auton Neurosci. 2014 Oct;185:120-2
pubmed: 25135040
Brain Stimul. 2014 Nov-Dec;7(6):871-7
pubmed: 25164906
Brain Stimul. 2017 Sep - Oct;10(5):875-881
pubmed: 28566194
Brain Res Bull. 2000 Sep 1;53(1):95-104
pubmed: 11033213
Hum Brain Mapp. 2016 Oct;37(10):3544-56
pubmed: 27168407
Brain Res. 1984 Feb 6;292(2):199-205
pubmed: 6692153
Anat Sci Int. 2014 Sep;89(4):238-45
pubmed: 24604237
J Comp Neurol. 1992 Jan 1;315(1):34-52
pubmed: 1371780
Brain Stimul. 2018 May - Jun;11(3):492-500
pubmed: 29361441
Pain. 2017 Aug;158(8):1461-1472
pubmed: 28541256
Cogn Affect Behav Neurosci. 2018 Aug;18(4):730-738
pubmed: 29713957
Front Hum Neurosci. 2014 Feb 28;8:116
pubmed: 24616692
Brain Stimul. 2019 Sep - Oct;12(5):1151-1158
pubmed: 31129152
Anesth Analg. 2018 Jun;126(6):2085-2092
pubmed: 29337730
Front Neurosci. 2019 Aug 09;13:854
pubmed: 31447643
Brain Stimul. 2019 May - Jun;12(3):824-826
pubmed: 30871845
Brain Stimul. 2019 Jul - Aug;12(4):911-921
pubmed: 30803865
Childs Nerv Syst. 2000 Feb;16(2):101-2
pubmed: 10663816
Brain Stimul. 2013 Sep;6(5):798-804
pubmed: 23453934
Annu Int Conf IEEE Eng Med Biol Soc. 2017 Jul;2017:3130-3133
pubmed: 29060561
Brain Stimul. 2015 May-Jun;8(3):624-36
pubmed: 25573069
J Neural Transm (Vienna). 2013 May;120(5):821-7
pubmed: 23117749
Front Hum Neurosci. 2013 Oct 04;7:623
pubmed: 24109446
Clin Neurophysiol. 2018 Nov;129(11):2503-2504
pubmed: 30249501
Neuroimage. 2018 Mar;168:412-426
pubmed: 28232189
Sci Rep. 2019 Aug 5;9(1):11305
pubmed: 31383932
Am J Physiol Heart Circ Physiol. 2005 Jan;288(1):H424-35
pubmed: 15374824
Philos Trans A Math Phys Eng Sci. 2016 May 13;374(2067):
pubmed: 27044996
Neuroimage. 2009 Feb 1;44(3):857-69
pubmed: 18951982
J Headache Pain. 2015;16:543
pubmed: 26156114
Neuroimage. 2008 Aug 1;42(1):169-77
pubmed: 18524629
Pain Med. 2012 Jun;13(6):777-89
pubmed: 22568773
J Clin Med. 2019 Apr 11;8(4):
pubmed: 30979068
Neuromodulation. 2017 Apr;20(3):290-300
pubmed: 27898202
Clin Neurophysiol. 2018 Nov;129(11):2501-2502
pubmed: 30268709
Front Neurosci. 2019 Jul 24;13:772
pubmed: 31396044
J Psychiatr Res. 2018 Jul;102:123-131
pubmed: 29674268
Science. 1991 Nov 1;254(5032):726-9
pubmed: 1683005
Cereb Cortex. 2016 Feb;26(2):485-97
pubmed: 25115821
Brain Stimul. 2018 Jul - Aug;11(4):699-708
pubmed: 29716843
Pain Rep. 2019 Aug 07;4(4):e745
pubmed: 31579846
Neuroimage. 2019 Aug 15;197:383-390
pubmed: 31055043
Int J Colorectal Dis. 2019 Mar;34(3):417-422
pubmed: 30519842
Clin Anat. 2002 Jan;15(1):35-7
pubmed: 11835542
Neuroimage. 2004 May;22(1):252-7
pubmed: 15110015

Auteurs

Roberta Sclocco (R)

Athinoula A. Martinos Center for Biomedical Imaging, Department of Radiology, Massachusetts General Hospital, Harvard Medical School, Charlestown, MA, USA; Department of Radiology, Logan University, Chesterfield, MO, USA. Electronic address: roberta@nmr.mgh.harvard.edu.

Ronald G Garcia (RG)

Athinoula A. Martinos Center for Biomedical Imaging, Department of Radiology, Massachusetts General Hospital, Harvard Medical School, Charlestown, MA, USA; Department of Psychiatry, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA; School of Medicine, Universidad de Santander (UDES), Bucaramanga, Colombia.

Norman W Kettner (NW)

Department of Radiology, Logan University, Chesterfield, MO, USA.

Harrison P Fisher (HP)

Athinoula A. Martinos Center for Biomedical Imaging, Department of Radiology, Massachusetts General Hospital, Harvard Medical School, Charlestown, MA, USA.

Kylie Isenburg (K)

Athinoula A. Martinos Center for Biomedical Imaging, Department of Radiology, Massachusetts General Hospital, Harvard Medical School, Charlestown, MA, USA.

Maya Makarovsky (M)

Athinoula A. Martinos Center for Biomedical Imaging, Department of Radiology, Massachusetts General Hospital, Harvard Medical School, Charlestown, MA, USA.

Jessica A Stowell (JA)

Department of Psychiatry, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA.

Jill Goldstein (J)

Athinoula A. Martinos Center for Biomedical Imaging, Department of Radiology, Massachusetts General Hospital, Harvard Medical School, Charlestown, MA, USA; Department of Psychiatry, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA; Department of Obstetrics and Gynecology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA.

Riccardo Barbieri (R)

Department of Electronics, Information and Bioengineering, Politecnico di Milano, Italy; Department of Anesthesia, Critical Care and Pain Medicine, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA.

Vitaly Napadow (V)

Athinoula A. Martinos Center for Biomedical Imaging, Department of Radiology, Massachusetts General Hospital, Harvard Medical School, Charlestown, MA, USA; Department of Radiology, Logan University, Chesterfield, MO, USA.

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