Central sensory-motor crosstalk in the neural gut-brain axis
The neural gut-brain axis consists of viscerosensory and autonomic motor neurons innervating the gastrointestinal (GI) tract. Sensory neurons transmit nutrient-related and non-nutrient-related information to the brain, while motor neurons regulate GI motility and secretion. Previous research provide...
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Veröffentlicht in: | Autonomic neuroscience 2020-05, Vol.225, p.102656-102656, Article 102656 |
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description | The neural gut-brain axis consists of viscerosensory and autonomic motor neurons innervating the gastrointestinal (GI) tract. Sensory neurons transmit nutrient-related and non-nutrient-related information to the brain, while motor neurons regulate GI motility and secretion. Previous research provides an incomplete picture of the brain nuclei that are directly connected with the neural gut-brain axis, and no studies have thoroughly assessed sensory-motor overlap in those nuclei. Our goal in this study was to comprehensively characterize the central sensory and motor circuitry associated with the neural gut-brain axis linked to a segment of the small intestine. We injected a retrograde (pseudorabies; PRV) and anterograde (herpes simplex virus 1; HSV) transsynaptic viral tracer into the duodenal wall of adult male rats. Immunohistochemical processing revealed single- and double-labeled cells that were quantified per nucleus. We found that across nearly all brain regions assessed, PRV + HSV immunoreactive neurons comprised the greatest percentage of labeled cells compared with single-labeled PRV or HSV neurons. These results indicate that even though sensory and motor information can be processed by separate neuronal populations, there is neuroanatomical evidence of direct sensory-motor feedback in the neural gut-brain axis throughout the entire caudal-rostral extent of the brain. This is the first study to exhaustively investigate the sensory-motor organization of the neural gut-brain axis, and is a step toward phenotyping the many central neuronal populations involved in GI control.
•Sensory and motor pathways of the gut-brain axis share common neurons in the brain.•These shared sensory-motor neurons exist in regions of the hind-, mid-, and forebrain.•Within nearly all regions assessed, ~50% of gut-brain neurons were sensory-motor neurons.•Central gut-brain neurons receiving sensory- or motor-only feedback were also observed.•These data provide an anatomical basis for sensory-motor feedback loops in the gut-brain axis. |
doi_str_mv | 10.1016/j.autneu.2020.102656 |
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•Sensory and motor pathways of the gut-brain axis share common neurons in the brain.•These shared sensory-motor neurons exist in regions of the hind-, mid-, and forebrain.•Within nearly all regions assessed, ~50% of gut-brain neurons were sensory-motor neurons.•Central gut-brain neurons receiving sensory- or motor-only feedback were also observed.•These data provide an anatomical basis for sensory-motor feedback loops in the gut-brain axis.</description><identifier>ISSN: 1566-0702</identifier><identifier>EISSN: 1872-7484</identifier><identifier>DOI: 10.1016/j.autneu.2020.102656</identifier><identifier>PMID: 32151980</identifier><language>eng</language><publisher>Netherlands: Elsevier B.V</publisher><subject>Autonomic nervous system ; Neuroanatomy ; Neuronal tract-tracers ; Small intestine ; Visceral afferents</subject><ispartof>Autonomic neuroscience, 2020-05, Vol.225, p.102656-102656, Article 102656</ispartof><rights>2020</rights><rights>Copyright © 2020. Published by Elsevier B.V.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c408t-d6a27644789ae844eb414682f873fed8fb4b8e01d7e85091403b3d8a2075088c3</citedby><cites>FETCH-LOGICAL-c408t-d6a27644789ae844eb414682f873fed8fb4b8e01d7e85091403b3d8a2075088c3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.autneu.2020.102656$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,780,784,3550,27924,27925,45995</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32151980$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Parker, Coltan G.</creatorcontrib><creatorcontrib>Dailey, Megan J.</creatorcontrib><creatorcontrib>Phillips, Heidi</creatorcontrib><creatorcontrib>Davis, Elizabeth A.</creatorcontrib><title>Central sensory-motor crosstalk in the neural gut-brain axis</title><title>Autonomic neuroscience</title><addtitle>Auton Neurosci</addtitle><description>The neural gut-brain axis consists of viscerosensory and autonomic motor neurons innervating the gastrointestinal (GI) tract. Sensory neurons transmit nutrient-related and non-nutrient-related information to the brain, while motor neurons regulate GI motility and secretion. Previous research provides an incomplete picture of the brain nuclei that are directly connected with the neural gut-brain axis, and no studies have thoroughly assessed sensory-motor overlap in those nuclei. Our goal in this study was to comprehensively characterize the central sensory and motor circuitry associated with the neural gut-brain axis linked to a segment of the small intestine. We injected a retrograde (pseudorabies; PRV) and anterograde (herpes simplex virus 1; HSV) transsynaptic viral tracer into the duodenal wall of adult male rats. Immunohistochemical processing revealed single- and double-labeled cells that were quantified per nucleus. We found that across nearly all brain regions assessed, PRV + HSV immunoreactive neurons comprised the greatest percentage of labeled cells compared with single-labeled PRV or HSV neurons. These results indicate that even though sensory and motor information can be processed by separate neuronal populations, there is neuroanatomical evidence of direct sensory-motor feedback in the neural gut-brain axis throughout the entire caudal-rostral extent of the brain. This is the first study to exhaustively investigate the sensory-motor organization of the neural gut-brain axis, and is a step toward phenotyping the many central neuronal populations involved in GI control.
•Sensory and motor pathways of the gut-brain axis share common neurons in the brain.•These shared sensory-motor neurons exist in regions of the hind-, mid-, and forebrain.•Within nearly all regions assessed, ~50% of gut-brain neurons were sensory-motor neurons.•Central gut-brain neurons receiving sensory- or motor-only feedback were also observed.•These data provide an anatomical basis for sensory-motor feedback loops in the gut-brain axis.</description><subject>Autonomic nervous system</subject><subject>Neuroanatomy</subject><subject>Neuronal tract-tracers</subject><subject>Small intestine</subject><subject>Visceral afferents</subject><issn>1566-0702</issn><issn>1872-7484</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><recordid>eNp9kE1LxDAQhoMo7rr6D0R69NJ1kqZJCiLI4hcseNFzSNupZu3HmqTi_ntbqx49zTA8My_zEHJKYUmBiovN0vShxX7JgI0jJlKxR-ZUSRZLrvj-0KdCxCCBzciR9xsAUJCJQzJLGE1ppmBOLlfYBmfqyGPrO7eLmy50Lipc530w9Vtk2yi8YjQEjdRLH-LcmWFoPq0_JgeVqT2e_NQFeb69eVrdx-vHu4fV9TouOKgQl8IwKTiXKjOoOMecUy4Uq5RMKixVlfNcIdBSokohoxySPCmVYSBTUKpIFuR8urt13XuPPujG-gLr2rTY9V6zRKYZQMLlgPIJ_f7AYaW3zjbG7TQFPXrTGz1506M3PXkb1s5-Evq8wfJv6VfUAFxNAA5_flh02hcW2wJL67AIuuzs_wlfEqR_MA</recordid><startdate>20200501</startdate><enddate>20200501</enddate><creator>Parker, Coltan G.</creator><creator>Dailey, Megan J.</creator><creator>Phillips, Heidi</creator><creator>Davis, Elizabeth A.</creator><general>Elsevier B.V</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope></search><sort><creationdate>20200501</creationdate><title>Central sensory-motor crosstalk in the neural gut-brain axis</title><author>Parker, Coltan G. ; Dailey, Megan J. ; Phillips, Heidi ; Davis, Elizabeth A.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c408t-d6a27644789ae844eb414682f873fed8fb4b8e01d7e85091403b3d8a2075088c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Autonomic nervous system</topic><topic>Neuroanatomy</topic><topic>Neuronal tract-tracers</topic><topic>Small intestine</topic><topic>Visceral afferents</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Parker, Coltan G.</creatorcontrib><creatorcontrib>Dailey, Megan J.</creatorcontrib><creatorcontrib>Phillips, Heidi</creatorcontrib><creatorcontrib>Davis, Elizabeth A.</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Autonomic neuroscience</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Parker, Coltan G.</au><au>Dailey, Megan J.</au><au>Phillips, Heidi</au><au>Davis, Elizabeth A.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Central sensory-motor crosstalk in the neural gut-brain axis</atitle><jtitle>Autonomic neuroscience</jtitle><addtitle>Auton Neurosci</addtitle><date>2020-05-01</date><risdate>2020</risdate><volume>225</volume><spage>102656</spage><epage>102656</epage><pages>102656-102656</pages><artnum>102656</artnum><issn>1566-0702</issn><eissn>1872-7484</eissn><abstract>The neural gut-brain axis consists of viscerosensory and autonomic motor neurons innervating the gastrointestinal (GI) tract. Sensory neurons transmit nutrient-related and non-nutrient-related information to the brain, while motor neurons regulate GI motility and secretion. Previous research provides an incomplete picture of the brain nuclei that are directly connected with the neural gut-brain axis, and no studies have thoroughly assessed sensory-motor overlap in those nuclei. Our goal in this study was to comprehensively characterize the central sensory and motor circuitry associated with the neural gut-brain axis linked to a segment of the small intestine. We injected a retrograde (pseudorabies; PRV) and anterograde (herpes simplex virus 1; HSV) transsynaptic viral tracer into the duodenal wall of adult male rats. Immunohistochemical processing revealed single- and double-labeled cells that were quantified per nucleus. We found that across nearly all brain regions assessed, PRV + HSV immunoreactive neurons comprised the greatest percentage of labeled cells compared with single-labeled PRV or HSV neurons. These results indicate that even though sensory and motor information can be processed by separate neuronal populations, there is neuroanatomical evidence of direct sensory-motor feedback in the neural gut-brain axis throughout the entire caudal-rostral extent of the brain. This is the first study to exhaustively investigate the sensory-motor organization of the neural gut-brain axis, and is a step toward phenotyping the many central neuronal populations involved in GI control.
•Sensory and motor pathways of the gut-brain axis share common neurons in the brain.•These shared sensory-motor neurons exist in regions of the hind-, mid-, and forebrain.•Within nearly all regions assessed, ~50% of gut-brain neurons were sensory-motor neurons.•Central gut-brain neurons receiving sensory- or motor-only feedback were also observed.•These data provide an anatomical basis for sensory-motor feedback loops in the gut-brain axis.</abstract><cop>Netherlands</cop><pub>Elsevier B.V</pub><pmid>32151980</pmid><doi>10.1016/j.autneu.2020.102656</doi><tpages>1</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Autonomic nervous system Neuroanatomy Neuronal tract-tracers Small intestine Visceral afferents |
title | Central sensory-motor crosstalk in the neural gut-brain axis |
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