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Cardiovascular autonomic effects of transcutaneous auricular nerve stimulation via the tragus in the rat involve spinal cervical sensory afferent pathways.

Abstract

BACKGROUND

Electrical stimulation on select areas of the external auricular dermatome influences the autonomic nervous system. It has been postulated that activation of the Auricular Branch of the Vagus Nerve (ABVN) mediates such autonomic changes. However, the underlying neural pathways mediating these effects are unknown and, further, our understanding of the anatomical distribution of the ABVN in the auricle has now been questioned.

OBJECTIVE

To investigate the effects of electrical stimulation of the tragus on autonomic outputs in the rat and probe the underlying neural pathways.

METHODS

Central neuronal projections from nerves innervating the external auricle were investigated by injections of the transganglionic tracer cholera toxin B chain (CTB) into the right tragus of Wistar rats. Physiological recordings of heart rate, perfusion pressure, respiratory rate and sympathetic nerve activity were made in an anaesthetic free Working Heart Brainstem Preparation (WHBP) of the rat and changes in response to electrical stimulation of the tragus analysed.

RESULTS

Neuronal tracing from the tragus revealed that the densest CTB labelling was within laminae III-IV of the dorsal horn of the upper cervical spinal cord, ipsilateral to the injection sites. In the medulla oblongata, CTB labelled afferents were observed in the paratrigeminal nucleus, spinal trigeminal tract and cuneate nucleus. Surprisingly, only sparse labelling was observed in the vagal afferent termination site, the nucleus tractus solitarius. Recordings made from rats at night time revealed more robust sympathetic activity in comparison to day time rats, thus subsequent experiments were conducted in rats at night time. Electrical stimulation was delivered across the tragus for 5 min. Direct recording from the sympathetic chain revealed a central sympathoinhibition by up to 36% following tragus stimulation. Sympathoinhibition remained following sectioning of the cervical vagus nerve ipsilateral to the stimulation site, but was attenuated by sectioning of the upper cervical afferent nerve roots.

CONCLUSIONS

Inhibition of the sympathetic nervous system activity upon electrical stimulation of the tragus in the rat is mediated at least in part through sensory afferent projections to the upper cervical spinal cord. This challenges the notion that tragal stimulation is mediated by the auricular branch of the vagus nerve and suggests that alternative mechanisms may be involved.

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  • Authors+Show Affiliations

    ,

    Faculty of Biological Sciences, School of Biomedical Sciences, University of Leeds, United Kingdom; Drug and Herbal Research Centre, Faculty of Pharmacy, Universiti Kebangsaan Malaysia, Kuala Lumpur, Malaysia.

    ,

    Faculty of Biological Sciences, School of Biomedical Sciences, University of Leeds, United Kingdom.

    ,

    Faculty of Biological Sciences, School of Biomedical Sciences, University of Leeds, United Kingdom. Electronic address: s.a.deuchars@leeds.ac.uk.

    Faculty of Biological Sciences, School of Biomedical Sciences, University of Leeds, United Kingdom. Electronic address: j.deuchars@leeds.ac.uk.

    Source

    Brain stimulation : 2019 May 06 pg

    Pub Type(s)

    Journal Article

    Language

    eng

    PubMed ID

    31129152

    Citation

    Mahadi, K M., et al. "Cardiovascular Autonomic Effects of Transcutaneous Auricular Nerve Stimulation Via the Tragus in the Rat Involve Spinal Cervical Sensory Afferent Pathways." Brain Stimulation, 2019.
    Mahadi KM, Lall VK, Deuchars SA, et al. Cardiovascular autonomic effects of transcutaneous auricular nerve stimulation via the tragus in the rat involve spinal cervical sensory afferent pathways. Brain Stimul. 2019.
    Mahadi, K. M., Lall, V. K., Deuchars, S. A., & Deuchars, J. (2019). Cardiovascular autonomic effects of transcutaneous auricular nerve stimulation via the tragus in the rat involve spinal cervical sensory afferent pathways. Brain Stimulation, doi:10.1016/j.brs.2019.05.002.
    Mahadi KM, et al. Cardiovascular Autonomic Effects of Transcutaneous Auricular Nerve Stimulation Via the Tragus in the Rat Involve Spinal Cervical Sensory Afferent Pathways. Brain Stimul. 2019 May 6; PubMed PMID: 31129152.
    * Article titles in AMA citation format should be in sentence-case
    TY - JOUR T1 - Cardiovascular autonomic effects of transcutaneous auricular nerve stimulation via the tragus in the rat involve spinal cervical sensory afferent pathways. AU - Mahadi,K M, AU - Lall,V K, AU - Deuchars,S A, AU - Deuchars,J, Y1 - 2019/05/06/ PY - 2018/11/22/received PY - 2019/04/17/revised PY - 2019/05/02/accepted PY - 2019/5/27/entrez KW - Auricular branch of the vagus nerve KW - Autonomic nervous system KW - Transcutaneous vagus nerve stimulation KW - Working heart brainstem preparation JF - Brain stimulation JO - Brain Stimul N2 - BACKGROUND: Electrical stimulation on select areas of the external auricular dermatome influences the autonomic nervous system. It has been postulated that activation of the Auricular Branch of the Vagus Nerve (ABVN) mediates such autonomic changes. However, the underlying neural pathways mediating these effects are unknown and, further, our understanding of the anatomical distribution of the ABVN in the auricle has now been questioned. OBJECTIVE: To investigate the effects of electrical stimulation of the tragus on autonomic outputs in the rat and probe the underlying neural pathways. METHODS: Central neuronal projections from nerves innervating the external auricle were investigated by injections of the transganglionic tracer cholera toxin B chain (CTB) into the right tragus of Wistar rats. Physiological recordings of heart rate, perfusion pressure, respiratory rate and sympathetic nerve activity were made in an anaesthetic free Working Heart Brainstem Preparation (WHBP) of the rat and changes in response to electrical stimulation of the tragus analysed. RESULTS: Neuronal tracing from the tragus revealed that the densest CTB labelling was within laminae III-IV of the dorsal horn of the upper cervical spinal cord, ipsilateral to the injection sites. In the medulla oblongata, CTB labelled afferents were observed in the paratrigeminal nucleus, spinal trigeminal tract and cuneate nucleus. Surprisingly, only sparse labelling was observed in the vagal afferent termination site, the nucleus tractus solitarius. Recordings made from rats at night time revealed more robust sympathetic activity in comparison to day time rats, thus subsequent experiments were conducted in rats at night time. Electrical stimulation was delivered across the tragus for 5 min. Direct recording from the sympathetic chain revealed a central sympathoinhibition by up to 36% following tragus stimulation. Sympathoinhibition remained following sectioning of the cervical vagus nerve ipsilateral to the stimulation site, but was attenuated by sectioning of the upper cervical afferent nerve roots. CONCLUSIONS: Inhibition of the sympathetic nervous system activity upon electrical stimulation of the tragus in the rat is mediated at least in part through sensory afferent projections to the upper cervical spinal cord. This challenges the notion that tragal stimulation is mediated by the auricular branch of the vagus nerve and suggests that alternative mechanisms may be involved. SN - 1876-4754 UR - https://www.unboundmedicine.com/medline/citation/31129152/Cardiovascular_autonomic_effects_of_transcutaneous_auricular_nerve_stimulation_via_the_tragus_in_the_rat_involve_spinal_cervical_sensory_afferent_pathways L2 - https://linkinghub.elsevier.com/retrieve/pii/S1935-861X(19)30208-6 DB - PRIME DP - Unbound Medicine ER -