Viscerosensory input drives angiotensin II type 1A receptor-expressing neurons in the solitary tract nucleus
Homeostatic regulation of visceral organ function requires integrated processing of neural and neurohormonal sensory signals. The nucleus of the solitary tract (NTS) is the primary sensory nucleus for cranial visceral sensory afferents. Angiotensin II (ANG II) is known to modulate peripheral viscera...
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Published in | American journal of physiology. Regulatory, integrative and comparative physiology Vol. 314; no. 2; pp. R282 - R293 |
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Main Authors | , , , , , , |
Format | Journal Article |
Language | English |
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United States
01.02.2018
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Abstract | Homeostatic regulation of visceral organ function requires integrated processing of neural and neurohormonal sensory signals. The nucleus of the solitary tract (NTS) is the primary sensory nucleus for cranial visceral sensory afferents. Angiotensin II (ANG II) is known to modulate peripheral visceral reflexes, in part, by activating ANG II type 1A receptors (AT
R) in the NTS. AT
R-expressing NTS neurons occur throughout the NTS with a defined subnuclear distribution, and most of these neurons are depolarized by ANG II. In this study we determined whether AT
R-expressing NTS neurons receive direct visceral sensory input, and whether this input is modulated by ANG II. Using AT
R-GFP mice to make targeted whole cell recordings from AT
R-expressing NTS neurons, we demonstrate that two-thirds (37 of 56) of AT
R-expressing neurons receive direct excitatory, visceral sensory input. In half of the neurons tested (4 of 8) the excitatory visceral sensory input was significantly reduced by application of the transient receptor potential vallinoid type 1 receptor agonist, capsaicin, indicating AT
R-expressing neurons can receive either C- or A-fiber-mediated input. Application of ANG II to a subset of second-order AT
R-expressing neurons did not affect spontaneous, evoked, or asynchronous glutamate release from visceral sensory afferents. Thus it is unlikely that AT
R-expressing viscerosensory neurons terminate on AT
R-expressing NTS neurons. Our data suggest that ANG II is likely to modulate multiple visceral sensory modalities by altering the excitability of second-order AT
R-expressing NTS neurons. |
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AbstractList | Homeostatic regulation of visceral organ function requires integrated processing of neural and neurohormonal sensory signals. The nucleus of the solitary tract (NTS) is the primary sensory nucleus for cranial visceral sensory afferents. Angiotensin II (ANG II) is known to modulate peripheral visceral reflexes, in part, by activating ANG II type 1A receptors (AT
1A
R) in the NTS. AT
1A
R-expressing NTS neurons occur throughout the NTS with a defined subnuclear distribution, and most of these neurons are depolarized by ANG II. In this study we determined whether AT
1A
R-expressing NTS neurons receive direct visceral sensory input, and whether this input is modulated by ANG II. Using AT
1A
R-GFP mice to make targeted whole cell recordings from AT
1A
R-expressing NTS neurons, we demonstrate that two-thirds (37 of 56) of AT
1A
R-expressing neurons receive direct excitatory, visceral sensory input. In half of the neurons tested (4 of 8) the excitatory visceral sensory input was significantly reduced by application of the transient receptor potential vallinoid type 1 receptor agonist, capsaicin, indicating AT
1A
R-expressing neurons can receive either C- or A-fiber-mediated input. Application of ANG II to a subset of second-order AT
1A
R-expressing neurons did not affect spontaneous, evoked, or asynchronous glutamate release from visceral sensory afferents. Thus it is unlikely that AT
1A
R-expressing viscerosensory neurons terminate on AT
1A
R-expressing NTS neurons. Our data suggest that ANG II is likely to modulate multiple visceral sensory modalities by altering the excitability of second-order AT
1A
R-expressing NTS neurons. Homeostatic regulation of visceral organ function requires integrated processing of neural and neurohormonal sensory signals. The nucleus of the solitary tract (NTS) is the primary sensory nucleus for cranial visceral sensory afferents. Angiotensin II (ANG II) is known to modulate peripheral visceral reflexes, in part, by activating ANG II type 1A receptors (AT R) in the NTS. AT R-expressing NTS neurons occur throughout the NTS with a defined subnuclear distribution, and most of these neurons are depolarized by ANG II. In this study we determined whether AT R-expressing NTS neurons receive direct visceral sensory input, and whether this input is modulated by ANG II. Using AT R-GFP mice to make targeted whole cell recordings from AT R-expressing NTS neurons, we demonstrate that two-thirds (37 of 56) of AT R-expressing neurons receive direct excitatory, visceral sensory input. In half of the neurons tested (4 of 8) the excitatory visceral sensory input was significantly reduced by application of the transient receptor potential vallinoid type 1 receptor agonist, capsaicin, indicating AT R-expressing neurons can receive either C- or A-fiber-mediated input. Application of ANG II to a subset of second-order AT R-expressing neurons did not affect spontaneous, evoked, or asynchronous glutamate release from visceral sensory afferents. Thus it is unlikely that AT R-expressing viscerosensory neurons terminate on AT R-expressing NTS neurons. Our data suggest that ANG II is likely to modulate multiple visceral sensory modalities by altering the excitability of second-order AT R-expressing NTS neurons. |
Author | Fong, A Y Connelly, A A McDougall, S J Guo, H Allen, A M Carter, D A Bassi, J K |
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SubjectTerms | Angiotensin II - pharmacology Animals Genes, Reporter Glutamic Acid - metabolism Green Fluorescent Proteins - genetics Green Fluorescent Proteins - metabolism Membrane Potentials Mice, Transgenic Nerve Fibers, Myelinated - metabolism Nerve Fibers, Unmyelinated - metabolism Neurons, Afferent - drug effects Neurons, Afferent - metabolism Promoter Regions, Genetic Receptor, Angiotensin, Type 1 - agonists Receptor, Angiotensin, Type 1 - genetics Receptor, Angiotensin, Type 1 - metabolism Solitary Nucleus - cytology Solitary Nucleus - drug effects Solitary Nucleus - metabolism Synaptic Transmission |
Title | Viscerosensory input drives angiotensin II type 1A receptor-expressing neurons in the solitary tract nucleus |
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