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 in | Neurogastroenterology and motility Vol. 32; no. 11; pp. e13925 - n/a |
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Main Authors | , , , , , , , , , |
Format | Journal Article |
Language | English |
Published |
Oxford
Wiley Subscription Services, Inc
01.11.2020
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Subjects | |
Online Access | Get full text |
ISSN | 1350-1925 1365-2982 1365-2982 |
DOI | 10.1111/nmo.13925 |
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Abstract | 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. |
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AbstractList | 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. 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.BACKGROUNDKnowledge 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.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.METHODSIn 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.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.KEY RESULTSDirect 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.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.CONCLUSION AND INFERENCESIn 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. BackgroundKnowledge 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.MethodsIn 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 ResultsDirect 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 InferencesIn 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. |
Author | Larauche, Muriel Wang, Po‐Min Liu, Wentai Dunn, James C. Y. Dubrovsky, Genia Million, Mulugeta Wang, Yushan Lo, Yi‐Kai Hsiang, En‐Lin Taché, Yvette |
AuthorAffiliation | 3 Department of Bioengineering, California NanoSystems Institute, UCLA, Los Angeles, CA, USA 1 CURE: Digestive Diseases Research Center (DDRCC), Center for Neurobiology of Stress and Resilience (CNSR), Vatche and Tamar Manoukian Division of Digestive Diseases, Department of Medicine, David Geffen School of Medicine, University of California Los Angeles, Los Angeles, CA, USA 2 VA Greater Los Angeles Healthcare System, Los Angeles, CA, USA 4 Department of Surgery, UCLA, Los Angeles, CA, USA 5 Departments of Surgery and Bioengineering, Stanford University, Stanford, CA, USA |
AuthorAffiliation_xml | – name: 1 CURE: Digestive Diseases Research Center (DDRCC), Center for Neurobiology of Stress and Resilience (CNSR), Vatche and Tamar Manoukian Division of Digestive Diseases, Department of Medicine, David Geffen School of Medicine, University of California Los Angeles, Los Angeles, CA, USA – name: 3 Department of Bioengineering, California NanoSystems Institute, UCLA, Los Angeles, CA, USA – name: 4 Department of Surgery, UCLA, Los Angeles, CA, USA – name: 2 VA Greater Los Angeles Healthcare System, Los Angeles, CA, USA – name: 5 Departments of Surgery and Bioengineering, Stanford University, Stanford, CA, USA |
Author_xml | – sequence: 1 givenname: Muriel orcidid: 0000-0003-3320-3675 surname: Larauche fullname: Larauche, Muriel organization: VA Greater Los Angeles Healthcare System – sequence: 2 givenname: Yushan surname: Wang fullname: Wang, Yushan organization: UCLA – sequence: 3 givenname: Po‐Min surname: Wang fullname: Wang, Po‐Min organization: UCLA – sequence: 4 givenname: Genia surname: Dubrovsky fullname: Dubrovsky, Genia organization: UCLA – sequence: 5 givenname: Yi‐Kai surname: Lo fullname: Lo, Yi‐Kai organization: UCLA – sequence: 6 givenname: En‐Lin surname: Hsiang fullname: Hsiang, En‐Lin organization: UCLA – sequence: 7 givenname: James C. Y. surname: Dunn fullname: Dunn, James C. Y. organization: Stanford University – sequence: 8 givenname: Yvette surname: Taché fullname: Taché, Yvette organization: VA Greater Los Angeles Healthcare System – sequence: 9 givenname: Wentai surname: Liu fullname: Liu, Wentai email: wentai@ucla.edu organization: UCLA – sequence: 10 givenname: Mulugeta surname: Million fullname: Million, Mulugeta email: millionmulugeta@mednet.ucla.edu organization: VA Greater Los Angeles Healthcare System |
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Notes | 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. ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 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 |
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Knowledge on optimal electrical stimulation (ES) modalities and region‐specific functional effects of colonic neuromodulation is lacking. We aimed... BackgroundKnowledge on optimal electrical stimulation (ES) modalities and region‐specific functional effects of colonic neuromodulation is lacking. We aimed to... Knowledge on optimal electrical stimulation (ES) modalities and region-specific functional effects of colonic neuromodulation is lacking. We aimed to map the... |
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SubjectTerms | celiac branch of the abdominal vagus nerve Colon Electrical stimuli electroceuticals functional mapping manometry Motility Muscle contraction Neural networks Neuromodulation Pressure Sensory neurons Vagus nerve |
Title | The effect of colonic tissue electrical stimulation and celiac branch of the abdominal vagus nerve neuromodulation on colonic motility in anesthetized pigs |
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