A revised conceptual framework for mouse vomeronasal pumping and stimulus sampling
Current Biology, vol. 34, pp. 1206–1221.e6
Abstract
The physiological performance of any sensory organ is determined by its anatomy and physical properties. Consequently, complex sensory structures with elaborate features have evolved to optimize stimulus detection. Understanding these structures and their physical nature forms the basis for mechanistic insights into sensory function. Despite its crucial role as a sensor for pheromones and other behaviorally instructive chemical cues, the vomeronasal organ (VNO) remains a poorly characterized mammalian sensory structure. Fundamental principles of its physico-mechanical function, including basic aspects of stimulus sampling, remain poorly explored. Here, we revisit the classical vasomotor pump hypothesis of vomeronasal stimulus uptake. Using advanced anatomical, histological, and physiological methods, we demonstrate that large parts of the lateral mouse VNO are composed of smooth muscle. Vomeronasal smooth muscle tissue comprises two subsets of fibers with distinct topography, structure, excitation-contraction coupling, and, ultimately, contractile properties. Specifically, contractions of a large population of noradrenaline-sensitive cells mediate both transverse and longitudinal lumen expansion, whereas cholinergic stimulation targets an adluminal group of smooth muscle fibers. The latter run parallel to the VNO's rostro-caudal axis and are ideally situated to mediate antagonistic longitudinal constriction of the lumen. This newly discovered arrangement implies a novel mode of function. Single-cell transcriptomics and pharmacological profiling reveal the receptor subtypes involved. Finally, 2D/3D tomography provides non-invasive insight into the intact VNO's anatomy and mechanics, enables measurement of luminal fluid volume, and allows an assessment of relative volume change upon noradrenergic stimulation. Together, we propose a revised conceptual framework for mouse vomeronasal pumping and, thus, stimulus sampling.
Authors 17
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Affiliation as printed
Department of Chemosensation, Institute for Biology II, RWTH Aachen University, 52074 Aachen, Germany
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Affiliation as printed
Department of Chemosensation, Institute for Biology II, RWTH Aachen University, 52074 Aachen, Germany; Research Training Group 2416 MultiSenses - MultiScales, RWTH Aachen University, 52074 Aachen, Germany
, RWTH Aachen University, 52074 Aachen, Germany
Department of Chemosensation, Institute for Biology II, RWTH Aachen University, 52074 Aachen, Germany
MultiSenses – MultiScales
Research Training Group 2416
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Affiliation as printed
Department of Chemosensation, Institute for Biology II, RWTH Aachen University, 52074 Aachen, Germany
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Affiliation as printed
Department of Chemosensation, Institute for Biology II, RWTH Aachen University, 52074 Aachen, Germany; Research Training Group 2416 MultiSenses - MultiScales, RWTH Aachen University, 52074 Aachen, Germany
, RWTH Aachen University, 52074 Aachen, Germany
Department of Chemosensation, Institute for Biology II, RWTH Aachen University, 52074 Aachen, Germany
MultiSenses – MultiScales
Research Training Group 2416
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Affiliation as printed
Department of Chemosensation, Institute for Biology II, RWTH Aachen University, 52074 Aachen, Germany
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University at Albany, State University of New York
Affiliation as printed
Department of Biological Sciences, The RNA Institute, University at Albany, Albany, NY 12222, USA
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Affiliation as printed
Department of Chemosensation, Institute for Biology II, RWTH Aachen University, 52074 Aachen, Germany
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Affiliation as printed
Institute of Imaging and Computer Vision, RWTH Aachen University, 52074 Aachen, Germany
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Howard Hughes Medical Institute · Harvard University
Affiliation as printed
Howard Hughes Medical Institute, Department of Cell Biology, Harvard Medical School, Boston, MA 02115, USA
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Enno Hachgenei Aachen Department of Production Metrology Fraunhofer Institute for Production Technology
Fraunhofer Institute for Production Technology IPT
Affiliation as printed
Department of Production Metrology, Fraunhofer Institute for Production Technology, 52074 Aachen, Germany
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Affiliation as printed
Department of Chemosensation, Institute for Biology II, RWTH Aachen University, 52074 Aachen, Germany
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Howard Hughes Medical Institute · Harvard University
Affiliation as printed
Howard Hughes Medical Institute, Department of Cell Biology, Harvard Medical School, Boston, MA 02115, USA
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Affiliation as printed
Research Training Group 2416 MultiSenses - MultiScales, RWTH Aachen University, 52074 Aachen, Germany; Institute of Imaging and Computer Vision, RWTH Aachen University, 52074 Aachen, Germany
, RWTH Aachen University, 52074 Aachen, Germany
Institute of Imaging and Computer Vision, RWTH Aachen University, 52074 Aachen, Germany
MultiSenses – MultiScales
Research Training Group 2416
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University at Albany, State University of New York
Affiliation as printed
Department of Biological Sciences, The RNA Institute, University at Albany, Albany, NY 12222, USA
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Affiliation as printed
Research Training Group 2416 MultiSenses - MultiScales, RWTH Aachen University, 52074 Aachen, Germany; Department of Neuroepigenetics, Institute for Biology II, RWTH Aachen University, 52074 Aachen, Germany
, RWTH Aachen University, 52074 Aachen, Germany
Department of Neuroepigenetics, Institute for Biology II, RWTH Aachen University, 52074 Aachen, Germany
MultiSenses – MultiScales
Research Training Group 2416
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Hebrew University of Jerusalem
Affiliation as printed
Department of Medical Neurobiology, Institute for Medical Research Israel Canada, Faculty of Medicine, The Hebrew University of Jerusalem, Jerusalem 9112102, Israel
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Affiliation as printed
Department of Chemosensation, Institute for Biology II, RWTH Aachen University, 52074 Aachen, Germany; Research Training Group 2416 MultiSenses - MultiScales, RWTH Aachen University, 52074 Aachen, Germany. Electronic address: m.spehr@sensorik.rwth-aachen.de
, RWTH Aachen University, 52074 Aachen, Germany
Department of Chemosensation, Institute for Biology II, RWTH Aachen University, 52074 Aachen, Germany
MultiSenses – MultiScales
Research Training Group 2416
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