Arterial Baroreceptors Sense Blood Pressure through Decorated Aortic Claws

Soohong Min,Rui B Chang,Sara L Prescott,Brennan Beeler,Narendra R Joshi,David E Strochlic,Stephen D Liberles

doi:10.1016/j.celrep.2019.10.040

Abstract

Mechanosensory neurons across physiological systems sense force using diverse terminal morphologies. Arterial baroreceptors are sensory neurons that monitor blood pressure for real-time stabilization of cardiovascular output. Various aortic sensory terminals have been described, but those that sense blood pressure are unclear because of a lack of selective genetic tools. Here, we find that all baroreceptor neurons are marked in Piezo2-ires-Cre mice and then use genetic approaches to visualize the architecture of mechanosensory endings. Cre-guided ablation of vagal and glossopharyngeal PIEZO2 neurons eliminates the baroreceptor reflex and aortic depressor nerve effects on blood pressure and heart rate. Genetic mapping reveals that PIEZO2 neurons form a distinctive mechanosensory structure: macroscopic claws that surround the aortic arch and exude fine end-net endings. Other arterial sensory neurons that form flower-spray terminals are dispensable for baroreception. Together, these findings provide structural insights into how blood pressure is sensed in the aortic vessel wall.

Highlights

Sensory neurons densely innervate the great vessels of the vascular system, providing essential moment-by-moment feedback for control of heart rate, blood pressure, and respiration
We find that blood pressure is sensed by mechanosensory neurons with macroscopic claws that circumnavigate the aortic arch and are laterally adorned with end-net endings
Genetic Identification of Baroreceptor Neurons through Optogenetics In prior studies, we generated a large collection of Cre knockin mice that target different subtypes of vagal sensory neurons and adapted genetic approaches for cell-specific neural mapping and optogenetics (Chang et al, 2015; Williams et al, 2016)

Summary

Introduction

Sensory neurons densely innervate the great vessels of the vascular system, providing essential moment-by-moment feedback for control of heart rate, blood pressure, and respiration. One classic cardiovascular reflex is the baroreceptor reflex, where elevated blood pressure instantaneously triggers compensatory decreases in cardiovascular output to steady blood flow to the brain and body (Benarroch, 2008; Brown, 1980; Kirchheim, 1976; Kumada et al, 1990; Wehrwein and Joyner, 2013). A description of baroreceptor morphology is lacking and is needed to understand mechanisms of force sensation by neurons within the arterial wall. Blood pressure sensation occurs at several hotspots within the vascular system. Afferents of the vagus nerve (cranial nerve 10) and glossopharyngeal nerve (cranial nerve 9) target the aortic arch and carotid sinus, respectively. Vagal and glossopharyngeal ganglia are fused into nodose/jugular/petrosal (NJP)

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