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Cited by 60Neuroscience of respiration and sleepNeurobiology and Insect Physiology ResearchMarine Invertebrate Physiology and Ecology

Serotonergic sensory-motor neurons mediate a behavioral response to hypoxia in pond snail embryos

Kuang, Shihuan, Doran, Shandra A., Wilson, Richard J. A., Goss, Greg G., Goldberg, Jeffrey I.·2002·Journal of Neurobiology
DOI 10.1002/neu.10071
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Abstract

Oxygen (O(2)) is one of the most important environmental factors that affects both physiological processes and development of aerobic animals, yet little is known about the neural mechanism of O(2) sensing and adaptive responses to low O(2) (hypoxia) during development. In the pond snail, Helisoma trivolvis, the first embryonic neurons (ENC1s) to develop are a pair of serotonergic sensory-motor cells that regulate a cilia-driven rotational behavior. Here, we report that the ENC1-ciliary cell circuit mediates an adaptive behavioral response to hypoxia. Exposure of egg masses to hypoxia elicited a dose-dependent and reversible acceleration of embryonic rotation that mixed capsular fluid, thereby facilitating O(2) diffusion to the embryo. The O(2) partial pressures (Po(2)) for threshold, half-maximal, and maximal rotational response were 60, 28, and 13 mm Hg, respectively. During hypoxia, embryos relocated to the periphery of the egg masses where higher Po(2) levels occurred. Furthermore, intermittent hypoxia treatments induced a sensitization of the rotational response. In isolated ciliary cells, ciliary beating was unaffected by hypoxia, suggesting that in the embryo, O(2) sensing occurs upstream of the motile cilia. The rotational response of embryos to hypoxia was attenuated by application of the serotonin receptor antagonist, mianserin, correlated to the development of ENC1-ciliary cell circuit, and abolished by laser-ablation of ENC1s. Together, these data suggest that ENC1s are unique oxygen sensors that may provide a good single cell model for the examination of mechanistic, developmental, and evolutionary aspects of O(2) sensing.

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  • In the embryos of the pond snail Helisoma trivolvis, sensory cells directly innervate the ciliated cells and accelerate ciliary beating via the release of serotonin upon hypoxic stimulation in the egg capsule.

    “Here sensory cells directly innervate the ciliated cells of the embryo and accelerate ciliary beating via the release of serotonin upon hypoxic stimulation in the egg capsule [46].”

    From Origin and early evolution of neural circuits for the control of ciliary locomotion (2011) · cites this paper as [46]

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Authors
Kuang, S., Doran, S. A., Wilson, R. J. A., Goss, G. G., & Goldberg, J. I.
Affiliations
  • University of Alberta (CA)
  • University of Calgary (CA)
Corresponding author
Goldberg, Jeffrey I.
ORCID
Venue
Journal of Neurobiology
Publisher
Wiley
Published
2002-06-17
Volume
52
Issue
1
Pages
73-83
ISSN
  • 0022-3034 (ISSN-L)
  • 1097-4695
DOI
10.1002/neu.10071
OpenAlex
W2058713755
Cited by
60
References
39
Citations by year
2024: 3 · 2023: 2 · 2022: 2 · 2021: 2 · 2020: 3 · 2019: 1 · 2017: 2 · 2016: 3 · 2015: 2 · 2014: 3 · 2013: 1 · 2012: 4
FWCI
1.05
Type
journal article
Language
en
Open access
closed
Licence
onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations
  • Journal of Neurobiology (publishedVersion)
  • PubMed (publishedVersion)
Topics
  • Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroscience of respiration and sleep
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
  • Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
Keywords
hypoxia, oxygen sensing, serotonergic neurons, Helisoma trivolvis, embryonic development, embryonic behavior, mianserin, serotonin receptors, laser ablation, intermittent hypoxia, egg weight
MeSH terms
Animals, Hypoxia, Behavior, Animal, Cells, Cultured, Embryo, Nonmammalian, Motor Neurons, Neurons, Afferent, Nitrogen, Oxygen, Serotonin, Snails

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