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Structure and Functions of the Vagus Nerve in Mammals

Matteo M. Ottaviani, Vaughan G. Macefield

10.1002/cphy.c210042

Source: Volume 12, Issue 4, October 2022

Published online: August 2022

Full Article on Wiley Online Library



Abstract

We review the structure and function of the vagus nerve, drawing on information obtained in humans and experimental animals. The vagus nerve is the largest and longest cranial nerve, supplying structures in the neck, thorax, and abdomen. It is also the only cranial nerve in which the vast majority of its innervation territory resides outside the head. While belonging to the parasympathetic division of the autonomic nervous system, the nerve is primarily sensory—it is dominated by sensory axons. We discuss the macroscopic and microscopic features of the nerve, including a detailed description of its extensive territory. Histochemical and genetic profiles of afferent and efferent axons are also detailed, as are the central nuclei involved in the processing of sensory information conveyed by the vagus nerve and the generation of motor (including parasympathetic) outflow via the vagus nerve. We provide a comprehensive review of the physiological roles of vagal sensory and motor neurons in control of the cardiovascular, respiratory, and gastrointestinal systems, and finish with a discussion on the interactions between the vagus nerve and the immune system. © 2022 American Physiological Society. Compr Physiol 12: 3989–4037, 2022.

Figure 1. Figure 1. General anatomy of the vagus nerve with all the major branches. Adapted with permission, from Ottaviani MM, et al., 2022 137/CCBY 4.0.
Figure 2. Figure 2. Thoracic vagus nerves with cervical and thoracic cardiac branches to the deep and superficial cardiac plexi and recurrent laryngeal nerves. Adapted with permission, from Ottaviani MM, et al., 2022 137/CCBY 4.0.
Figure 3. Figure 3. Thoracic vagus forming the esophageal plexus and then converging onto the anterior and posterior vagal trunks and major abdominal vagus nerves branches. Created with BioRender.com.
Figure 4. Figure 4. A histological transversal section of a pig cervical vagus nerve in hematoxylin and eosin staining.
Figure 5. Figure 5. Comparative anatomy of the cervical vagus nerve between mouse, rat, canine, nonhuman primate (NHP), pig, and human. Adapted, with permission, from Settell ML, et al., 2020 171 / IOP Publishing/CC BY 3.0.
Figure 6. Figure 6. Histological sections taken at several locations along the length of pig vagus nerve demonstrating bimodal organization or vagotopy. Section 1 was taken through the nodose ganglion and superior laryngeal branch and contains the pseudo‐unipolar cells aggregated in a large “fascicle” that gives rise to a distinct smaller grouping of fascicles in sections 2 to 4. After the recurrent laryngeal bifurcates from the vagus nerve trunk, the bimodal organization is no longer evident (section 5). Adapted, with permission, from Settell ML, et al., 2020 171/IOP Publishing/CC BY 3.0/CC BY 4.0.
Figure 7. Figure 7. Single‐cell RNA sequencing of murine nodose and jugular neurons and their hierarchical clusterization. (A) Vagal jugular and nodose neurons were distinguished via expression of Prdm12 and Phox2b proteins, respectively, and clustered based on gene expression of neurotransmitters, membrane receptors, and cytoskeletal proteins. These profiles were then compared to those of dorsal root ganglia (DRG) neurons for further functional classifications. (B) Jugular neurons were grouped into six clusters and classified as generic somatosensory neurons due to the similarities with the genetic profile of DRG neurons. (C) Nodose neurons were divided into 18 clusters with unique somatosensory profiles and were divided into two main groups including mechanosensory neurons (NG1‐11) and nociceptor‐like neurons (NG12‐18). Adapted, with permission, from Kupari et al. 2019 100/Springer Nature.
Figure 8. Figure 8. Proposed vagus nerve sensory neuron classification and their relation to function. (A) Jugular ganglion neuron types and their functional relations are based on shared neuronal identity with functionally characterized dorsal root ganglia neurons. (B) NG1–NG11 nodose ganglion mechanosensory‐like neurons molecular profiles. (C) Nodose ganglion nociceptor‐like neurons molecular profiles (NG12‐18). Adapted, with permission, from Kupari J, et al., 2019 100.
Figure 9. Figure 9. Comprehensive comparison of genetically defined vagal sensory neurons subpopulations and clusters among three different studies 6,101,204. Adapted, with permission, from Zhao Q, et al., 2022 204/Springer Nature/CC BY 4.0.
Figure 10. Figure 10. (A) A single‐cell sequencing approach (Projection‐seq) based on multiplexed projection barcodes to generate genetic profiles of vagal sensory neurons innervating different visceral organs. (B) Comprehensive uniform manifold approximation and projection plot of vagal sensory neurons integrating the three feature‐coding dimensions such as the target organ (indicated by colored lines), the type of endings in tissue layers (indicated using italic), and the stimulus modality (labeled in bold). (C) Vagal sensory neurons have stereotypical endings along various tissue layers across multiple visceral organs. (D) Schematic explanation of the multidimensional coding architecture of the vagal interoceptive system. The three coding dimensions, such as visceral organ (red), tissue layer (blue), and sensory modality (green), specify parallel sensory pathways combined to precisely and effectively present body signals to the brain. These sensory pathways are no longer organized in serial, but in a more complex divergent and convergent manner in the brainstem, based on multiple features of interoceptive signals. Adapted, with permission, from Zhao Q, et al., 2022 204.
Figure 11. Figure 11. (A) Rostro‐caudal distribution of central autonomic network components in the central nervous system. (B) Schematic representation of the central autonomic network with internuclei connections. An autonomic vagovagal loop comprises visceral inputs to the nucleus tractus solitarii (NTS) which then sends outputs to the dorsal motor nucleus (DMNV), the rostral ventrolateral medullary (RVLM), and the intermediate lateral medulla (ILM) to adapt the autonomic balance to physiological demands. This autonomic forebrain loop is modulated by a forebrain autonomic loop, through cross‐talk between the NTS and brain areas (hypothalamus, amygdala, cingulate cortex, insula, prefrontal cortex) that are also involved in neuroendocrine, emotional, and cognitive controls of behavior. (C) Distribution of the major visceral terminations in the NTS. AP, area postrema. Created with BioRender.com.
Figure 12. Figure 12. (A) Piezo2+ vagal fibers with a ring‐like morphology visualized with immunofluorescence in thick coronal aortic sections in a Piezo2‐ires‐Cre mice; scale bar, 100 μm. (B) Piezo2+ neurons visualized by confocal microscopy represent a subset of fibers in the aortic depressor nerve, with all neurons visualized by immunofluorescence for synaptophysin (blue); scale bar, 20 μm. (A,B) Adapted, with permission, from Min S, et al., 2019 127. (C) Immunofluorescence visualization of murine vagal baroreceptor with, from left to right, end‐net endings, club ending, and surround the entire aorta with a schematic illustration on the right. Scale bars: 50 μm. Adapted, with permission, from Lu H‐J, et al., 2020 110; Min S, et al., 2019 127. (D) Immunofluorescent double staining of flower spray baroreceptors terminals with leaf‐like or knob‐like terminal expansions. Adapted, with permission, from Liu J, et al., 2021 108. (E) Imaging pipeline of vagal afferent terminals in the intact cleared heart using nodose ganglia injection of AAV‐FLEX‐tdTomato in corresponding Cre mouse lines. (F) Distribution of the three vagal afferent ending types in the heart. Purple circles, plate of puncta (flower spray) endings; blue squares, parallel intramuscular arrays; orange circles, varicose surface endings. (G) Representative cardiovascular vagal endings. RA, right atrium; LA, left atrium; RCV, right cardiac vein; AO, aorta; PT, pulmonary trunk. Adapted, with permission, from Zhao Q, et al., 2022 204.
Figure 13. Figure 13. Scheme of neural discharges of the best characterized cardiopulmonary vagal afferent fibers in the literature. Rhythmic discharges of vagal fibers are shown in relationship to physiological parameters (ECG, BP, CVP, and RESP). BP, blood pressure; CVP, central venous pressure with a corresponding to atrial contraction, c to tricuspid valve bulging into the right atrium, x to right atrium relaxation, v to the rapid filling of the right atrium, and y to early ventricular filling; RESP, respiration; bR, aortic baroreceptors; AaR, type A atrial receptors; BaR, type B atrial receptors; SAR, slowly adapting pulmonary receptors; RAR, rapidly, adapting pulmonary receptor.
Figure 14. Figure 14. (A) Schematic representation of thoracic cardiovascular afferent fibers traveling in the vagus nerve with their distribution to target tissues and their main myelination profiles. Cardiovascular afferent fibers include baro‐ and chemoreceptors from the aortic arch and the bifurcation of the right brachiocephalic trunk, left and right atrial, myocardial, and pericardial receptors. Insets: top, baroreceptors Piezo2+ and TTN3+ terminals; down, unmyelinated 5‐HT3R+ myocardial receptors involved in the Bezold‐Jarisch reflex. (B) Different vagal reflexes initiated via activation of cardiovascular vagal afferents. NTS, nucleus tractus solitarii; NA, nucleus ambiguous; RVLM, rostral ventrolateral medulla; CVLM, caudal ventrolateral medulla; VRG, ventral respiratory group. Created with BioRender.com.
Figure 15. Figure 15. (A) P2RY1 neuron terminals visualized in an open‐book preparation of the larynx after injecting AAV‐flex‐AP into nodose and jugular ganglia of P2RY1‐ires‐Cre mice. Scale bar, 500 μm. (B) Diagram depicting terminals of various neuron types in the larynx after AAV mapping. (C) Representative images of P2RY1 terminals. Scale bars, 50 mm. (D) Taste buds visualized in larynx cryosections by KRT8 immunohistochemistry (green). Scale bar, 100 mm. (E) Two‐color immunohistochemistry for KRT8 (green) and tdTomato (magenta) in cryosections of the larynx from P2RY1‐ires‐Cre mice injected with AAV‐flex‐ tdTomato in nodose and jugular ganglia. Scale bar, 50 mm. Adapted, with permission, from Prescott SL, et al., 2020 154/Elsevier.
Figure 16. Figure 16. (A) Schematic representation of jugular and nodose neurons distribution in the airways and specific terminations of different classes of vagal afferent and efferent fibers in the airways wall. (B) Circuitry of pulmonary reflexes involving SARs and RARs activation. SARs stimulation by lung inflation causes the Hering‐Breuer reflex with activation of the ventral respiratory group (VRG) that promotes expiration, and inhibition of the dorsal respiratory group (DRG) that stimulate inspiration. SARs activation causes also inhibition of the vagal cardiac outflow, leading to reflex tachycardia and reduction in systemic vascular resistance. RARs activation increases breathing frequency and parasympathetic outflow to the lungs causing reflex bronchoconstriction and airway mucus secretion. AC, apneustic center. Created with BioRender.com.
Figure 17. Figure 17. (A) Different populations of nodose neurons innervating the gastrointestinal tract. (B) Scheme of vagal innervation of the gut wall. (C) Distribution of specific vagal afferent populations along the gut. The color code is the same as in (A). Created with BioRender.com.
Figure 18. Figure 18. The vagus nerve connectome in the immune system. mAChR, muscarinic acetylcholine receptor; AChE, acetylcholine esterase; AP, area postrema; RVLM, rostral ventrolateral medulla; DA, dopamine; NG, nodose ganglion; CG, celiac ganglia; HPA, hypothalamic‐pituitary‐adrenal axis; PVN, paraventricular nucleus; NE, norepinephrine. Created with BioRender.com.


Figure 1. General anatomy of the vagus nerve with all the major branches. Adapted with permission, from Ottaviani MM, et al., 2022 137/CCBY 4.0.


Figure 2. Thoracic vagus nerves with cervical and thoracic cardiac branches to the deep and superficial cardiac plexi and recurrent laryngeal nerves. Adapted with permission, from Ottaviani MM, et al., 2022 137/CCBY 4.0.


Figure 3. Thoracic vagus forming the esophageal plexus and then converging onto the anterior and posterior vagal trunks and major abdominal vagus nerves branches. Created with BioRender.com.


Figure 4. A histological transversal section of a pig cervical vagus nerve in hematoxylin and eosin staining.


Figure 5. Comparative anatomy of the cervical vagus nerve between mouse, rat, canine, nonhuman primate (NHP), pig, and human. Adapted, with permission, from Settell ML, et al., 2020 171 / IOP Publishing/CC BY 3.0.


Figure 6. Histological sections taken at several locations along the length of pig vagus nerve demonstrating bimodal organization or vagotopy. Section 1 was taken through the nodose ganglion and superior laryngeal branch and contains the pseudo‐unipolar cells aggregated in a large “fascicle” that gives rise to a distinct smaller grouping of fascicles in sections 2 to 4. After the recurrent laryngeal bifurcates from the vagus nerve trunk, the bimodal organization is no longer evident (section 5). Adapted, with permission, from Settell ML, et al., 2020 171/IOP Publishing/CC BY 3.0/CC BY 4.0.


Figure 7. Single‐cell RNA sequencing of murine nodose and jugular neurons and their hierarchical clusterization. (A) Vagal jugular and nodose neurons were distinguished via expression of Prdm12 and Phox2b proteins, respectively, and clustered based on gene expression of neurotransmitters, membrane receptors, and cytoskeletal proteins. These profiles were then compared to those of dorsal root ganglia (DRG) neurons for further functional classifications. (B) Jugular neurons were grouped into six clusters and classified as generic somatosensory neurons due to the similarities with the genetic profile of DRG neurons. (C) Nodose neurons were divided into 18 clusters with unique somatosensory profiles and were divided into two main groups including mechanosensory neurons (NG1‐11) and nociceptor‐like neurons (NG12‐18). Adapted, with permission, from Kupari et al. 2019 100/Springer Nature.


Figure 8. Proposed vagus nerve sensory neuron classification and their relation to function. (A) Jugular ganglion neuron types and their functional relations are based on shared neuronal identity with functionally characterized dorsal root ganglia neurons. (B) NG1–NG11 nodose ganglion mechanosensory‐like neurons molecular profiles. (C) Nodose ganglion nociceptor‐like neurons molecular profiles (NG12‐18). Adapted, with permission, from Kupari J, et al., 2019 100.


Figure 9. Comprehensive comparison of genetically defined vagal sensory neurons subpopulations and clusters among three different studies 6,101,204. Adapted, with permission, from Zhao Q, et al., 2022 204/Springer Nature/CC BY 4.0.


Figure 10. (A) A single‐cell sequencing approach (Projection‐seq) based on multiplexed projection barcodes to generate genetic profiles of vagal sensory neurons innervating different visceral organs. (B) Comprehensive uniform manifold approximation and projection plot of vagal sensory neurons integrating the three feature‐coding dimensions such as the target organ (indicated by colored lines), the type of endings in tissue layers (indicated using italic), and the stimulus modality (labeled in bold). (C) Vagal sensory neurons have stereotypical endings along various tissue layers across multiple visceral organs. (D) Schematic explanation of the multidimensional coding architecture of the vagal interoceptive system. The three coding dimensions, such as visceral organ (red), tissue layer (blue), and sensory modality (green), specify parallel sensory pathways combined to precisely and effectively present body signals to the brain. These sensory pathways are no longer organized in serial, but in a more complex divergent and convergent manner in the brainstem, based on multiple features of interoceptive signals. Adapted, with permission, from Zhao Q, et al., 2022 204.


Figure 11. (A) Rostro‐caudal distribution of central autonomic network components in the central nervous system. (B) Schematic representation of the central autonomic network with internuclei connections. An autonomic vagovagal loop comprises visceral inputs to the nucleus tractus solitarii (NTS) which then sends outputs to the dorsal motor nucleus (DMNV), the rostral ventrolateral medullary (RVLM), and the intermediate lateral medulla (ILM) to adapt the autonomic balance to physiological demands. This autonomic forebrain loop is modulated by a forebrain autonomic loop, through cross‐talk between the NTS and brain areas (hypothalamus, amygdala, cingulate cortex, insula, prefrontal cortex) that are also involved in neuroendocrine, emotional, and cognitive controls of behavior. (C) Distribution of the major visceral terminations in the NTS. AP, area postrema. Created with BioRender.com.


Figure 12. (A) Piezo2+ vagal fibers with a ring‐like morphology visualized with immunofluorescence in thick coronal aortic sections in a Piezo2‐ires‐Cre mice; scale bar, 100 μm. (B) Piezo2+ neurons visualized by confocal microscopy represent a subset of fibers in the aortic depressor nerve, with all neurons visualized by immunofluorescence for synaptophysin (blue); scale bar, 20 μm. (A,B) Adapted, with permission, from Min S, et al., 2019 127. (C) Immunofluorescence visualization of murine vagal baroreceptor with, from left to right, end‐net endings, club ending, and surround the entire aorta with a schematic illustration on the right. Scale bars: 50 μm. Adapted, with permission, from Lu H‐J, et al., 2020 110; Min S, et al., 2019 127. (D) Immunofluorescent double staining of flower spray baroreceptors terminals with leaf‐like or knob‐like terminal expansions. Adapted, with permission, from Liu J, et al., 2021 108. (E) Imaging pipeline of vagal afferent terminals in the intact cleared heart using nodose ganglia injection of AAV‐FLEX‐tdTomato in corresponding Cre mouse lines. (F) Distribution of the three vagal afferent ending types in the heart. Purple circles, plate of puncta (flower spray) endings; blue squares, parallel intramuscular arrays; orange circles, varicose surface endings. (G) Representative cardiovascular vagal endings. RA, right atrium; LA, left atrium; RCV, right cardiac vein; AO, aorta; PT, pulmonary trunk. Adapted, with permission, from Zhao Q, et al., 2022 204.


Figure 13. Scheme of neural discharges of the best characterized cardiopulmonary vagal afferent fibers in the literature. Rhythmic discharges of vagal fibers are shown in relationship to physiological parameters (ECG, BP, CVP, and RESP). BP, blood pressure; CVP, central venous pressure with a corresponding to atrial contraction, c to tricuspid valve bulging into the right atrium, x to right atrium relaxation, v to the rapid filling of the right atrium, and y to early ventricular filling; RESP, respiration; bR, aortic baroreceptors; AaR, type A atrial receptors; BaR, type B atrial receptors; SAR, slowly adapting pulmonary receptors; RAR, rapidly, adapting pulmonary receptor.


Figure 14. (A) Schematic representation of thoracic cardiovascular afferent fibers traveling in the vagus nerve with their distribution to target tissues and their main myelination profiles. Cardiovascular afferent fibers include baro‐ and chemoreceptors from the aortic arch and the bifurcation of the right brachiocephalic trunk, left and right atrial, myocardial, and pericardial receptors. Insets: top, baroreceptors Piezo2+ and TTN3+ terminals; down, unmyelinated 5‐HT3R+ myocardial receptors involved in the Bezold‐Jarisch reflex. (B) Different vagal reflexes initiated via activation of cardiovascular vagal afferents. NTS, nucleus tractus solitarii; NA, nucleus ambiguous; RVLM, rostral ventrolateral medulla; CVLM, caudal ventrolateral medulla; VRG, ventral respiratory group. Created with BioRender.com.


Figure 15. (A) P2RY1 neuron terminals visualized in an open‐book preparation of the larynx after injecting AAV‐flex‐AP into nodose and jugular ganglia of P2RY1‐ires‐Cre mice. Scale bar, 500 μm. (B) Diagram depicting terminals of various neuron types in the larynx after AAV mapping. (C) Representative images of P2RY1 terminals. Scale bars, 50 mm. (D) Taste buds visualized in larynx cryosections by KRT8 immunohistochemistry (green). Scale bar, 100 mm. (E) Two‐color immunohistochemistry for KRT8 (green) and tdTomato (magenta) in cryosections of the larynx from P2RY1‐ires‐Cre mice injected with AAV‐flex‐ tdTomato in nodose and jugular ganglia. Scale bar, 50 mm. Adapted, with permission, from Prescott SL, et al., 2020 154/Elsevier.


Figure 16. (A) Schematic representation of jugular and nodose neurons distribution in the airways and specific terminations of different classes of vagal afferent and efferent fibers in the airways wall. (B) Circuitry of pulmonary reflexes involving SARs and RARs activation. SARs stimulation by lung inflation causes the Hering‐Breuer reflex with activation of the ventral respiratory group (VRG) that promotes expiration, and inhibition of the dorsal respiratory group (DRG) that stimulate inspiration. SARs activation causes also inhibition of the vagal cardiac outflow, leading to reflex tachycardia and reduction in systemic vascular resistance. RARs activation increases breathing frequency and parasympathetic outflow to the lungs causing reflex bronchoconstriction and airway mucus secretion. AC, apneustic center. Created with BioRender.com.


Figure 17. (A) Different populations of nodose neurons innervating the gastrointestinal tract. (B) Scheme of vagal innervation of the gut wall. (C) Distribution of specific vagal afferent populations along the gut. The color code is the same as in (A). Created with BioRender.com.


Figure 18. The vagus nerve connectome in the immune system. mAChR, muscarinic acetylcholine receptor; AChE, acetylcholine esterase; AP, area postrema; RVLM, rostral ventrolateral medulla; DA, dopamine; NG, nodose ganglion; CG, celiac ganglia; HPA, hypothalamic‐pituitary‐adrenal axis; PVN, paraventricular nucleus; NE, norepinephrine. Created with BioRender.com.
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Article Title: Structure and Functions of the Vagus Nerve in Mammals
 

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Matteo M. Ottaviani, Vaughan G. Macefield. Structure and Functions of the Vagus Nerve in Mammals. Compr Physiol 2022, 12: 3989-4037. doi: 10.1002/cphy.c210042