Robust Estimation of Respiratory Variability Uncovers Correlates of Limbic Brain Activity and Transcutaneous Cervical Vagus Nerve Stimulation in the Context of Traumatic Stress

Overview

Journal IEEE Trans Biomed Eng

Specialties Biomedical Engineering
Biophysics

Date 2021 Aug 27

PMID 34449355

Citations 12

Authors

Asim H Gazi

Matthew T Wittbrodt

Anna B Harrison

Srirakshaa Sundararaj

Nil Z Gurel

Jonathon A Nye

Amit J Shah

Viola Vaccarino

J Douglas Bremner

Omer T Inan

Affiliations

Soon will be listed here.

Abstract

Objective: Variations in respiration patterns are a characteristic response to distress due to underlying neurorespiratory couplings. Yet, no work to date has quantified respiration pattern variability (RPV) in the context of traumatic stress and studied its functional neural correlates - this analysis aims to address this gap.

Methods: Fifty human subjects with prior traumatic experiences (24 with posttraumatic stress disorder (PTSD)) completed a ∼3-hr protocol involving personalized traumatic scripts and active/sham (double-blind) transcutaneous cervical vagus nerve stimulation (tcVNS). High-resolution positron emission tomography functional neuroimages, electrocardiogram (ECG), and respiratory effort (RSP) data were collected during the protocol. Supplementing the RSP signal with ECG-derived respiration for quality assessment and timing extraction, RPV metrics were quantified and analyzed. Specifically, correlation analyses were performed using neuroactivity in selected limbic regions, and responses to active and sham tcVNS were compared.

Results: The single-lag unscaled autocorrelation of respiration rate correlated negatively with left amygdala activity and positively with right rostromedial prefrontal cortex (rmPFC) activity for non-PTSD; it also correlated negatively with left and right insulae activity and positively with right rmPFC activity for PTSD. The single-lag unscaled autocorrelation of expiration time was greater following active stimulation for non-PTSD.

Conclusion: Quantifying RPV is of demonstrable importance to assessing trauma-induced changes in neural function and tcVNS effects on respiratory physiology.

Significance: This is the first demonstration of RPV's pertinence to traumatic stress- and tcVNS-induced neurorespiratory responses. The open-source processing pipeline elucidated herein uniquely includes both RSP and ECG-derived respiration signals for quality assessment, timing estimation, and RPV extraction.

Citing Articles

Transcutaneous vagus nerve stimulation: a bibliometric study on current research hotspots and status.

Fan S, Yan L, Zhang J, Sun Y, Qian Y, Wang M Front Neurosci. 2024; 18:1406135.

PMID: 39221007 PMC: 11363710. DOI: 10.3389/fnins.2024.1406135.

Posttraumatic Stress Disorder and Obstructive Sleep Apnea in Twins.

Shah A, Vaccarino V, Goldberg J, Huang M, Ko Y, Ma X JAMA Netw Open. 2024; 7(6):e2416352.

PMID: 38913378 PMC: 11197451. DOI: 10.1001/jamanetworkopen.2024.16352.

Quantifying Posttraumatic Stress Disorder Symptoms During Traumatic Memories Using Interpretable Markers of Respiratory Variability.

Gazi A, Sanchez-Perez J, Saks G, Alday E, Haffar A, Ahmed H IEEE J Biomed Health Inform. 2024; 28(8):4912-4924.

PMID: 38713564 PMC: 11364449. DOI: 10.1109/JBHI.2024.3397589.

Noninvasive Vagal Nerve Stimulation for Opioid Use Disorder.

Douglas Bremner J, Gazi A, Lambert T, Nawar A, Harrison A, Welsh J Ann Depress Anxiety. 2023; 10(1).

PMID: 38074313 PMC: 10699253.

Transcutaneous auricular Vagus Nerve Stimulation and Median Nerve Stimulation reduce acute stress in young healthy adults: a single-blind sham-controlled crossover study.

Sanchez-Perez J, Gazi A, Rahman F, Seith A, Saks G, Sundararaj S Front Neurosci. 2023; 17:1213982.

PMID: 37746156 PMC: 10512834. DOI: 10.3389/fnins.2023.1213982.

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