Cytokine-specific Neurograms in the Sensory Vagus Nerve
Abstract The axons of the sensory, or afferent, vagus nerve transmit action potentials to the central nervous system in response to changes in the body’s metabolic and physiological status. Recent advances in identifying neural circuits that regulate immune responses to infection, inflammation and i...
| Main Authors: | , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2016-12-01
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| Series: | Bioelectronic Medicine |
| Online Access: | http://link.springer.com/article/10.15424/bioelectronmed.2016.00007 |
| _version_ | 1828531053318373376 |
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| author | Benjamin E. Steinberg Harold A. Silverman Sergio Robbiati Manoj K. Gunasekaran Téa Tsaava Emily Battinelli Andrew Stiegler Chad E. Bouton Sangeeta S. Chavan Kevin J. Tracey Patricio T. Huerta |
| author_facet | Benjamin E. Steinberg Harold A. Silverman Sergio Robbiati Manoj K. Gunasekaran Téa Tsaava Emily Battinelli Andrew Stiegler Chad E. Bouton Sangeeta S. Chavan Kevin J. Tracey Patricio T. Huerta |
| author_sort | Benjamin E. Steinberg |
| collection | DOAJ |
| description | Abstract The axons of the sensory, or afferent, vagus nerve transmit action potentials to the central nervous system in response to changes in the body’s metabolic and physiological status. Recent advances in identifying neural circuits that regulate immune responses to infection, inflammation and injury have revealed that vagus nerve signals regulate the release of cytokines and other factors produced by macrophages. Here we record compound action potentials in the cervical vagus nerve of adult mice and reveal the specific activity that occurs following administration of the proinflammatory cytokines tumor necrosis factor (TNF) and interleukin 1β (IL-1β). Importantly, the afferent vagus neurograms generated by TNF exposure are abolished in double knockout mice lacking TNF receptors 1 and 2 (TNF-R1/2KO), whereas IL-1 β-specific neurograms are eliminated in knockout mice lacking IL-1 β receptor (IL-1RKO). Conversely, TNF neurograms are preserved in IL-1RKO mice, and IL-1 β neurograms are unchanged in TNF-R1/2KO mice. Analysis of the temporal dynamics and power spectral characteristics of afferent vagus neurograms for TNF and IL-1β reveals cytokine-selective signals. The nodose ganglion contains the cell bodies of the sensory neurons whose axons run through the vagus nerve. The nodose neurons express receptors for TNF and IL-1β, and we show that exposing them to TNF and IL-1β significantly stimulates their calcium uptake. Together these results indicate that afferent vagus signals in response to cytokines provide a basic model of nervous system sensing of immune responses. |
| first_indexed | 2024-12-11T22:32:04Z |
| format | Article |
| id | doaj.art-82e7f528c9314d10b323e8a3723b5551 |
| institution | Directory Open Access Journal |
| issn | 2332-8886 |
| language | English |
| last_indexed | 2024-12-11T22:32:04Z |
| publishDate | 2016-12-01 |
| publisher | BMC |
| record_format | Article |
| series | Bioelectronic Medicine |
| spelling | doaj.art-82e7f528c9314d10b323e8a3723b55512022-12-22T00:48:05ZengBMCBioelectronic Medicine2332-88862016-12-013171710.15424/bioelectronmed.2016.00007Cytokine-specific Neurograms in the Sensory Vagus NerveBenjamin E. Steinberg0Harold A. Silverman1Sergio Robbiati2Manoj K. Gunasekaran3Téa Tsaava4Emily Battinelli5Andrew Stiegler6Chad E. Bouton7Sangeeta S. Chavan8Kevin J. Tracey9Patricio T. Huerta10Laboratory of Biomedical Science, The Feinstein Institute for Medical Research, Northwell HealthLaboratory of Biomedical Science, The Feinstein Institute for Medical Research, Northwell HealthLaboratory of Immune and Neural Networks, The Feinstein Institute for Medical Research, Northwell HealthLaboratory of Biomedical Science, The Feinstein Institute for Medical Research, Northwell HealthLaboratory of Biomedical Science, The Feinstein Institute for Medical Research, Northwell HealthLaboratory of Biomedical Science, The Feinstein Institute for Medical Research, Northwell HealthCirculatory Technologies, Inc.Center for Bioelectronic Medicine, The Feinstein Institute for Medical Research, Northwell HealthLaboratory of Biomedical Science, The Feinstein Institute for Medical Research, Northwell HealthLaboratory of Biomedical Science, The Feinstein Institute for Medical Research, Northwell HealthLaboratory of Immune and Neural Networks, The Feinstein Institute for Medical Research, Northwell HealthAbstract The axons of the sensory, or afferent, vagus nerve transmit action potentials to the central nervous system in response to changes in the body’s metabolic and physiological status. Recent advances in identifying neural circuits that regulate immune responses to infection, inflammation and injury have revealed that vagus nerve signals regulate the release of cytokines and other factors produced by macrophages. Here we record compound action potentials in the cervical vagus nerve of adult mice and reveal the specific activity that occurs following administration of the proinflammatory cytokines tumor necrosis factor (TNF) and interleukin 1β (IL-1β). Importantly, the afferent vagus neurograms generated by TNF exposure are abolished in double knockout mice lacking TNF receptors 1 and 2 (TNF-R1/2KO), whereas IL-1 β-specific neurograms are eliminated in knockout mice lacking IL-1 β receptor (IL-1RKO). Conversely, TNF neurograms are preserved in IL-1RKO mice, and IL-1 β neurograms are unchanged in TNF-R1/2KO mice. Analysis of the temporal dynamics and power spectral characteristics of afferent vagus neurograms for TNF and IL-1β reveals cytokine-selective signals. The nodose ganglion contains the cell bodies of the sensory neurons whose axons run through the vagus nerve. The nodose neurons express receptors for TNF and IL-1β, and we show that exposing them to TNF and IL-1β significantly stimulates their calcium uptake. Together these results indicate that afferent vagus signals in response to cytokines provide a basic model of nervous system sensing of immune responses.http://link.springer.com/article/10.15424/bioelectronmed.2016.00007 |
| spellingShingle | Benjamin E. Steinberg Harold A. Silverman Sergio Robbiati Manoj K. Gunasekaran Téa Tsaava Emily Battinelli Andrew Stiegler Chad E. Bouton Sangeeta S. Chavan Kevin J. Tracey Patricio T. Huerta Cytokine-specific Neurograms in the Sensory Vagus Nerve Bioelectronic Medicine |
| title | Cytokine-specific Neurograms in the Sensory Vagus Nerve |
| title_full | Cytokine-specific Neurograms in the Sensory Vagus Nerve |
| title_fullStr | Cytokine-specific Neurograms in the Sensory Vagus Nerve |
| title_full_unstemmed | Cytokine-specific Neurograms in the Sensory Vagus Nerve |
| title_short | Cytokine-specific Neurograms in the Sensory Vagus Nerve |
| title_sort | cytokine specific neurograms in the sensory vagus nerve |
| url | http://link.springer.com/article/10.15424/bioelectronmed.2016.00007 |
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