Neural regulation of slow waves and phasic contractions in the distal stomach: a mathematical model
Neural regulation of gastric motility occurs partly through the regulation of gastric bioelectrical slow waves (SWs) and phasic contractions. The interaction of the tissues and organs involved in this regulatory process is complex. We sought to infer the relative importance of cellular mechanisms in...
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| Veröffentlicht in: | Journal of neural engineering 2023-12, Vol.20 (6), p.66040 |
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| container_title | Journal of neural engineering |
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| creator | Athavale, Omkar N Avci, Recep Clark, Alys R Di Natale, Madeleine R Wang, Xiaokai Furness, John B Liu, Zhongming Cheng, Leo K Du, Peng |
| description | Neural regulation of gastric motility occurs partly through the regulation of gastric bioelectrical slow waves (SWs) and phasic contractions. The interaction of the tissues and organs involved in this regulatory process is complex. We sought to infer the relative importance of cellular mechanisms in inhibitory neural regulation of the stomach by enteric neurons and the interaction of inhibitory and excitatory electrical field stimulation.
A novel mathematical model of gastric motility regulation by enteric neurons was developed and scenarios were simulated to determine the mechanisms through which enteric neural influence is exerted. This model was coupled to revised and extended electrophysiological models of gastric SWs and smooth muscle cells (SMCs).
The mathematical model predicted that regulation of contractile apparatus sensitivity to intracellular calcium in the SMC was the major inhibition mechanism of active tension development, and that the effect on SW amplitude depended on the inhibition of non-specific cation currents more than the inhibition of calcium-activated chloride current (k
= 0.77 vs k
= 0.33). The model predicted that the interaction between inhibitory and excitatory neural regulation, when applied with simultaneous and equal intensity, resulted in an inhibition of contraction amplitude almost equivalent to that of inhibitory stimulation (79% vs 77% decrease), while the effect on frequency was overall excitatory, though less than excitatory stimulation alone (66% vs 47% increase).
The mathematical model predicts the effects of inhibitory and excitatory enteric neural stimulation on gastric motility function, as well as the effects when inhibitory and excitatory enteric neural stimulation interact. Incorporation of the model into organ-level simulations will provide insights regarding pathological mechanisms that underpin gastric functional disorders, and allow for
testing of the effects of clinical neuromodulation protocols for the treatment of these disorders. |
| doi_str_mv | 10.1088/1741-2552/ad1610 |
| format | Article |
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A novel mathematical model of gastric motility regulation by enteric neurons was developed and scenarios were simulated to determine the mechanisms through which enteric neural influence is exerted. This model was coupled to revised and extended electrophysiological models of gastric SWs and smooth muscle cells (SMCs).
The mathematical model predicted that regulation of contractile apparatus sensitivity to intracellular calcium in the SMC was the major inhibition mechanism of active tension development, and that the effect on SW amplitude depended on the inhibition of non-specific cation currents more than the inhibition of calcium-activated chloride current (k
= 0.77 vs k
= 0.33). The model predicted that the interaction between inhibitory and excitatory neural regulation, when applied with simultaneous and equal intensity, resulted in an inhibition of contraction amplitude almost equivalent to that of inhibitory stimulation (79% vs 77% decrease), while the effect on frequency was overall excitatory, though less than excitatory stimulation alone (66% vs 47% increase).
The mathematical model predicts the effects of inhibitory and excitatory enteric neural stimulation on gastric motility function, as well as the effects when inhibitory and excitatory enteric neural stimulation interact. Incorporation of the model into organ-level simulations will provide insights regarding pathological mechanisms that underpin gastric functional disorders, and allow for
testing of the effects of clinical neuromodulation protocols for the treatment of these disorders.</description><identifier>ISSN: 1741-2560</identifier><identifier>EISSN: 1741-2552</identifier><identifier>DOI: 10.1088/1741-2552/ad1610</identifier><identifier>PMID: 38100816</identifier><identifier>CODEN: JNEOBH</identifier><language>eng</language><publisher>England: IOP Publishing</publisher><subject>autonomic neuroscience ; Calcium ; gastric electrophysiology ; gastric motility ; mathematical modelling ; Muscle Contraction - physiology ; Myocytes, Smooth Muscle ; Neurons ; Stomach - physiology</subject><ispartof>Journal of neural engineering, 2023-12, Vol.20 (6), p.66040</ispartof><rights>2024 The Author(s). Published by IOP Publishing Ltd</rights><rights>Creative Commons Attribution license.</rights><rights>2024 The Author(s). Published by IOP Publishing Ltd 2024</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c466t-d4e01fe65e75d30f0e3fdff5c5cacc80a4febe95ad923232414c606b78622edf3</citedby><cites>FETCH-LOGICAL-c466t-d4e01fe65e75d30f0e3fdff5c5cacc80a4febe95ad923232414c606b78622edf3</cites><orcidid>0000-0002-8773-4204 ; 0000-0003-0144-8053 ; 0000-0002-6913-7545 ; 0000-0003-2652-2192</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://iopscience.iop.org/article/10.1088/1741-2552/ad1610/pdf$$EPDF$$P50$$Giop$$Hfree_for_read</linktopdf><link.rule.ids>230,314,780,784,885,27924,27925,53846,53893</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38100816$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Athavale, Omkar N</creatorcontrib><creatorcontrib>Avci, Recep</creatorcontrib><creatorcontrib>Clark, Alys R</creatorcontrib><creatorcontrib>Di Natale, Madeleine R</creatorcontrib><creatorcontrib>Wang, Xiaokai</creatorcontrib><creatorcontrib>Furness, John B</creatorcontrib><creatorcontrib>Liu, Zhongming</creatorcontrib><creatorcontrib>Cheng, Leo K</creatorcontrib><creatorcontrib>Du, Peng</creatorcontrib><title>Neural regulation of slow waves and phasic contractions in the distal stomach: a mathematical model</title><title>Journal of neural engineering</title><addtitle>JNE</addtitle><addtitle>J. Neural Eng</addtitle><description>Neural regulation of gastric motility occurs partly through the regulation of gastric bioelectrical slow waves (SWs) and phasic contractions. The interaction of the tissues and organs involved in this regulatory process is complex. We sought to infer the relative importance of cellular mechanisms in inhibitory neural regulation of the stomach by enteric neurons and the interaction of inhibitory and excitatory electrical field stimulation.
A novel mathematical model of gastric motility regulation by enteric neurons was developed and scenarios were simulated to determine the mechanisms through which enteric neural influence is exerted. This model was coupled to revised and extended electrophysiological models of gastric SWs and smooth muscle cells (SMCs).
The mathematical model predicted that regulation of contractile apparatus sensitivity to intracellular calcium in the SMC was the major inhibition mechanism of active tension development, and that the effect on SW amplitude depended on the inhibition of non-specific cation currents more than the inhibition of calcium-activated chloride current (k
= 0.77 vs k
= 0.33). The model predicted that the interaction between inhibitory and excitatory neural regulation, when applied with simultaneous and equal intensity, resulted in an inhibition of contraction amplitude almost equivalent to that of inhibitory stimulation (79% vs 77% decrease), while the effect on frequency was overall excitatory, though less than excitatory stimulation alone (66% vs 47% increase).
The mathematical model predicts the effects of inhibitory and excitatory enteric neural stimulation on gastric motility function, as well as the effects when inhibitory and excitatory enteric neural stimulation interact. Incorporation of the model into organ-level simulations will provide insights regarding pathological mechanisms that underpin gastric functional disorders, and allow for
testing of the effects of clinical neuromodulation protocols for the treatment of these disorders.</description><subject>autonomic neuroscience</subject><subject>Calcium</subject><subject>gastric electrophysiology</subject><subject>gastric motility</subject><subject>mathematical modelling</subject><subject>Muscle Contraction - physiology</subject><subject>Myocytes, Smooth Muscle</subject><subject>Neurons</subject><subject>Stomach - physiology</subject><issn>1741-2560</issn><issn>1741-2552</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>O3W</sourceid><sourceid>EIF</sourceid><recordid>eNp1UU1v1DAQtaqifsG9J-RbObB07CRO0gtCFQWkCi5wHnntcderJE7tpBX_HoctqyKBLNnW83tvxvMYOxfwTkDTXIq6FCtZVfJSW6EEHLCTPXS4vys4ZqcpbQEKUbdwxI6LRgA0Qp0w85XmqDse6W7u9OTDwIPjqQuP_FE_UOJ6sHzc6OQNN2GYojYLKXE_8GlD3Po0ZXmaQq_N5opr3uuM582bjPfBUveSvXC6S_Tq6TxjP24-fr_-vLr99unL9YfblSmVmla2JBCOVEV1ZQtwQIWzzlWmMtqYBnTpaE1tpW0ri7xKURoFal03Skqyrjhj73e-47zuyRpa2u1wjL7X8ScG7fHvl8Fv8C48oIBaVVCU2eHNk0MM9zOlCXufDHWdHijMCWULslWNlG2mwo5qYkgpktvXEYBLOLhMH5ckcBdOlrx-3t9e8CeNTLjYEXwYcRvmOORx4XYglIAKQSkoAcffX337D-Z_K_8CXQ-n1Q</recordid><startdate>20231201</startdate><enddate>20231201</enddate><creator>Athavale, Omkar N</creator><creator>Avci, Recep</creator><creator>Clark, Alys R</creator><creator>Di Natale, Madeleine R</creator><creator>Wang, Xiaokai</creator><creator>Furness, John B</creator><creator>Liu, Zhongming</creator><creator>Cheng, Leo K</creator><creator>Du, Peng</creator><general>IOP Publishing</general><scope>O3W</scope><scope>TSCCA</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-8773-4204</orcidid><orcidid>https://orcid.org/0000-0003-0144-8053</orcidid><orcidid>https://orcid.org/0000-0002-6913-7545</orcidid><orcidid>https://orcid.org/0000-0003-2652-2192</orcidid></search><sort><creationdate>20231201</creationdate><title>Neural regulation of slow waves and phasic contractions in the distal stomach: a mathematical model</title><author>Athavale, Omkar N ; Avci, Recep ; Clark, Alys R ; Di Natale, Madeleine R ; Wang, Xiaokai ; Furness, John B ; Liu, Zhongming ; Cheng, Leo K ; Du, Peng</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c466t-d4e01fe65e75d30f0e3fdff5c5cacc80a4febe95ad923232414c606b78622edf3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>autonomic neuroscience</topic><topic>Calcium</topic><topic>gastric electrophysiology</topic><topic>gastric motility</topic><topic>mathematical modelling</topic><topic>Muscle Contraction - physiology</topic><topic>Myocytes, Smooth Muscle</topic><topic>Neurons</topic><topic>Stomach - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Athavale, Omkar N</creatorcontrib><creatorcontrib>Avci, Recep</creatorcontrib><creatorcontrib>Clark, Alys R</creatorcontrib><creatorcontrib>Di Natale, Madeleine R</creatorcontrib><creatorcontrib>Wang, Xiaokai</creatorcontrib><creatorcontrib>Furness, John B</creatorcontrib><creatorcontrib>Liu, Zhongming</creatorcontrib><creatorcontrib>Cheng, Leo K</creatorcontrib><creatorcontrib>Du, Peng</creatorcontrib><collection>IOP Publishing Free Content</collection><collection>IOPscience (Open Access)</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Journal of neural engineering</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Athavale, Omkar N</au><au>Avci, Recep</au><au>Clark, Alys R</au><au>Di Natale, Madeleine R</au><au>Wang, Xiaokai</au><au>Furness, John B</au><au>Liu, Zhongming</au><au>Cheng, Leo K</au><au>Du, Peng</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Neural regulation of slow waves and phasic contractions in the distal stomach: a mathematical model</atitle><jtitle>Journal of neural engineering</jtitle><stitle>JNE</stitle><addtitle>J. Neural Eng</addtitle><date>2023-12-01</date><risdate>2023</risdate><volume>20</volume><issue>6</issue><spage>66040</spage><pages>66040-</pages><issn>1741-2560</issn><eissn>1741-2552</eissn><coden>JNEOBH</coden><abstract>Neural regulation of gastric motility occurs partly through the regulation of gastric bioelectrical slow waves (SWs) and phasic contractions. The interaction of the tissues and organs involved in this regulatory process is complex. We sought to infer the relative importance of cellular mechanisms in inhibitory neural regulation of the stomach by enteric neurons and the interaction of inhibitory and excitatory electrical field stimulation.
A novel mathematical model of gastric motility regulation by enteric neurons was developed and scenarios were simulated to determine the mechanisms through which enteric neural influence is exerted. This model was coupled to revised and extended electrophysiological models of gastric SWs and smooth muscle cells (SMCs).
The mathematical model predicted that regulation of contractile apparatus sensitivity to intracellular calcium in the SMC was the major inhibition mechanism of active tension development, and that the effect on SW amplitude depended on the inhibition of non-specific cation currents more than the inhibition of calcium-activated chloride current (k
= 0.77 vs k
= 0.33). The model predicted that the interaction between inhibitory and excitatory neural regulation, when applied with simultaneous and equal intensity, resulted in an inhibition of contraction amplitude almost equivalent to that of inhibitory stimulation (79% vs 77% decrease), while the effect on frequency was overall excitatory, though less than excitatory stimulation alone (66% vs 47% increase).
The mathematical model predicts the effects of inhibitory and excitatory enteric neural stimulation on gastric motility function, as well as the effects when inhibitory and excitatory enteric neural stimulation interact. Incorporation of the model into organ-level simulations will provide insights regarding pathological mechanisms that underpin gastric functional disorders, and allow for
testing of the effects of clinical neuromodulation protocols for the treatment of these disorders.</abstract><cop>England</cop><pub>IOP Publishing</pub><pmid>38100816</pmid><doi>10.1088/1741-2552/ad1610</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0002-8773-4204</orcidid><orcidid>https://orcid.org/0000-0003-0144-8053</orcidid><orcidid>https://orcid.org/0000-0002-6913-7545</orcidid><orcidid>https://orcid.org/0000-0003-2652-2192</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
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| ispartof | Journal of neural engineering, 2023-12, Vol.20 (6), p.66040 |
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| language | eng |
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| source | MEDLINE; IOP Publishing Journals; Institute of Physics (IOP) Journals - HEAL-Link |
| subjects | autonomic neuroscience Calcium gastric electrophysiology gastric motility mathematical modelling Muscle Contraction - physiology Myocytes, Smooth Muscle Neurons Stomach - physiology |
| title | Neural regulation of slow waves and phasic contractions in the distal stomach: a mathematical model |
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