The effect of colonic tissue electrical stimulation and celiac branch of the abdominal vagus nerve neuromodulation on colonic motility in anesthetized pigs

Background Knowledge on optimal electrical stimulation (ES) modalities and region‐specific functional effects of colonic neuromodulation is lacking. We aimed to map the regional colonic motility in response to ES of (a) the colonic tissue and (b) celiac branch of the abdominal vagus nerve (CBVN) in...

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Published inNeurogastroenterology and motility Vol. 32; no. 11; pp. e13925 - n/a
Main Authors Larauche, Muriel, Wang, Yushan, Wang, Po‐Min, Dubrovsky, Genia, Lo, Yi‐Kai, Hsiang, En‐Lin, Dunn, James C. Y., Taché, Yvette, Liu, Wentai, Million, Mulugeta
Format Journal Article
LanguageEnglish
Published Oxford Wiley Subscription Services, Inc 01.11.2020
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ISSN1350-1925
1365-2982
1365-2982
DOI10.1111/nmo.13925

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Summary:Background Knowledge on optimal electrical stimulation (ES) modalities and region‐specific functional effects of colonic neuromodulation is lacking. We aimed to map the regional colonic motility in response to ES of (a) the colonic tissue and (b) celiac branch of the abdominal vagus nerve (CBVN) in an anesthetized porcine model. Methods In male Yucatan pigs, direct ES (10 Hz, 2 ms, 15 mA) of proximal (pC), transverse (tC), or distal (dC) colon was done using planar flexible multi‐electrode array panels and CBVN ES (2 Hz, 0.3‐4 ms, 5 mA) using pulse train (PT), continuous (10 min), or square‐wave (SW) modalities, with or without afferent nerve block (200 Hz, 0.1 ms, 2 mA). The regional luminal manometric changes were quantified as area under the curve of contractions (AUC) and luminal pressure maps generated. Contractions frequency power spectral analysis was performed. Contraction propagation was assessed using video animation of motility changes. Key Results Direct colon ES caused visible local circular (pC, tC) or longitudinal (dC) muscle contractions and increased luminal pressure AUC in pC, tC, and dC (143.0 ± 40.7%, 135.8 ± 59.7%, and 142.0 ± 62%, respectively). The colon displayed prominent phasic pressure frequencies ranging from 1 to 12 cpm. Direct pC and tC ES increased the dominant contraction frequency band (1‐6 cpm) power locally. Pulse train CBVN ES (2 Hz, 4 ms, 5 mA) triggered pancolonic contractions, reduced by concurrent afferent block. Colon contractions propagated both orally and aborally in short distances. Conclusion and Inferences In anesthetized pigs, the dominant contraction frequency band is 1‐6 cpm. Direct colonic ES causes primarily local contractions. The CBVN ES‐induced pancolonic contractions involve central neural network. In anesthetized male Yucatan pigs, direct colonic ES causes primarily local contractions while pulse train CBVN ES induces pancolonic contractions involving central neural network. This study provides a foundational basis to guide safe and effective neuromodulation for patients suffering from intractable colonic motility disorders.
Bibliography:Funding information
Part of the work was presented at the 3rd Meeting of the Federation of Neurogastroenterology and Motility and Postgraduate Course on Gastrointestinal Motility, 29 August‐1 September 2018, Amsterdam The Netherlands and the 11th Congress of International Society for Autonomic Neuroscience, July 25‐27 2019, Los Angeles, CA.
Muriel Larauche and Yushan Wang are Co‐first authors.
This work was supported by NIH OT2 OD024899 (PD/PI Y. Taché, Subaward PI: Million Mulugeta), the CURE: Digestive Diseases Research Center P30 DK 41301 (Animal Model Core; MM, YT, ML) and a VA Senior Research Career Scientist Award (YT). Wentai Liu and his Lab was also partially supported by an endowment fund of Chen Soon‐Shiong Bionic Engineering Center.
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Author contribution
Prof. Wentai Liu, PhD, Department of Bioengineering, California NanoSystems Institute, University of California Los Angeles, Los Angeles, CA, USA. wentai@ucla.edu
ML, PMW, YW, IH, GD, MM performed the experiments; YKL, WL, JD, YT provided key resources; ML, YW, MM, wrote the manuscript; WL, JD, YT did critical revision of the manuscript.
Co-first authors
ISSN:1350-1925
1365-2982
1365-2982
DOI:10.1111/nmo.13925