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PMID: 25246547 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Neuronal mechanism for acute mechanosensitivity in tactile-foraging waterfowl.

Schneider ER, Mastrotto M, Laursen WJ, Schulz VP, Goodman JB, Funk OH, Gallagher PG, Gracheva EO, Bagriantsev SN

Abstract

Relying almost exclusively on their acute sense of touch, tactile-foraging birds can feed in murky water, but the cellular mechanism is unknown. Mechanical stimuli activate specialized cutaneous end organs in the bill, innervated by trigeminal afferents. We report that trigeminal ganglia (TG) of domestic and wild tactile-foraging ducks exhibit numerical expansion of large-diameter mechanoreceptive neurons expressing the mechano-gated ion channel Piezo2. These features are not found in visually foraging birds. Moreover, in the duck, the expansion of mechanoreceptors occurs at the expense of thermosensors. Direct mechanical stimulation of duck TG neurons evokes high-amplitude depolarizing current with a low threshold of activation, high signal amplification gain, and slow kinetics of inactivation. Together, these factors contribute to efficient conversion of light mechanical stimuli into neuronal excitation. Our results reveal an evolutionary strategy to hone tactile perception in vertebrates at the level of primary afferents.

Keywords
Piezo2 TRPM8 TRPV1 mechanotransduction
MeSH Terms
Animals Down-Regulation Ducks/physiology Feeding Behavior Ion Channel Gating Ion Channels/metabolism Mechanotransduction, Cellular Neurons/physiology Sensory Thresholds TRPM Cation Channels/metabolism TRPV Cation Channels/metabolism Thermoreceptors/metabolism Touch/physiology Trigeminal Ganglion/physiology Up-Regulation
Chemicals
Ion Channels TRPM Cation Channels TRPV Cation Channels
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Schneider Eve R
Department of Cellular and Molecular Physiology.
Mastrotto Marco
Department of Cellular and Molecular Physiology, Yale Program in Cellular Neuroscience, Neurodegeneration and Repair.
Laursen Willem J
Department of Cellular and Molecular Physiology, Yale Program in Cellular Neuroscience, Neurodegeneration and Repair.
Schulz Vincent P
Department of Pediatrics, Yale University School of Medicine, New Haven, CT 06520.
Goodman Jena B
Department of Cellular and Molecular Physiology, Yale Program in Cellular Neuroscience, Neurodegeneration and Repair.
Funk Owen H
Department of Cellular and Molecular Physiology.
Gallagher Patrick G
Department of Pediatrics, Yale University School of Medicine, New Haven, CT 06520.
Gracheva Elena O
Department of Cellular and Molecular Physiology, Yale Program in Cellular Neuroscience, Neurodegeneration and Repair, sviatoslav.bagriantsev@yale.edu elena.gracheva@yale.edu.
Bagriantsev Sviatoslav N
Department of Cellular and Molecular Physiology, sviatoslav.bagriantsev@yale.edu elena.gracheva@yale.edu.
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Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
1091-6490
Published
2014-10-14
Epub
2014-00-22
Pages
14941-6
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC4205607
Subset
IM
Grants
NICHD NIH HHS · T32 HD007094 · United States
NCATS NIH HHS · UL1 TR000142 · United States
NHGRI NIH HHS · T32HG319810 · United States
NICHD NIH HHS · T32HD007094 · United States
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