A Cross-Species Analysis Reveals a General Role for Piezo2 in Mechanosensory Specialization of Trigeminal Ganglia from Tactile Specialist Birds
Eve R. Schneider,
Evan O. Anderson,
Viktor V. Feketa,
Marco Mastrotto,
Yury A. Nikolaev,
Elena O. Gracheva,
Sviatoslav N. Bagriantsev
Affiliations
Eve R. Schneider
Department of Cellular and Molecular Physiology, Yale University School of Medicine, 333 Cedar St., New Haven, CT 06510, USA
Evan O. Anderson
Department of Cellular and Molecular Physiology, Yale University School of Medicine, 333 Cedar St., New Haven, CT 06510, USA
Viktor V. Feketa
Department of Cellular and Molecular Physiology, Yale University School of Medicine, 333 Cedar St., New Haven, CT 06510, USA; Department of Neuroscience, Yale University School of Medicine, 333 Cedar St., New Haven, CT 06510, USA; Program in Cellular Neuroscience, Neurodegeneration and Repair, Yale University School of Medicine, 333 Cedar St., New Haven, CT 06510, USA
Marco Mastrotto
Department of Cellular and Molecular Physiology, Yale University School of Medicine, 333 Cedar St., New Haven, CT 06510, USA; Department of Neuroscience, Yale University School of Medicine, 333 Cedar St., New Haven, CT 06510, USA; Program in Cellular Neuroscience, Neurodegeneration and Repair, Yale University School of Medicine, 333 Cedar St., New Haven, CT 06510, USA
Yury A. Nikolaev
Department of Cellular and Molecular Physiology, Yale University School of Medicine, 333 Cedar St., New Haven, CT 06510, USA
Elena O. Gracheva
Department of Cellular and Molecular Physiology, Yale University School of Medicine, 333 Cedar St., New Haven, CT 06510, USA; Department of Neuroscience, Yale University School of Medicine, 333 Cedar St., New Haven, CT 06510, USA; Program in Cellular Neuroscience, Neurodegeneration and Repair, Yale University School of Medicine, 333 Cedar St., New Haven, CT 06510, USA; Corresponding author
Sviatoslav N. Bagriantsev
Department of Cellular and Molecular Physiology, Yale University School of Medicine, 333 Cedar St., New Haven, CT 06510, USA; Corresponding author
Summary: A major challenge in biology is to link cellular and molecular variations with behavioral phenotypes. Here, we studied somatosensory neurons from a panel of bird species from the family Anatidae, known for their tactile-based foraging behavior. We found that tactile specialists exhibit a proportional expansion of neuronal mechanoreceptors in trigeminal ganglia. The expansion of mechanoreceptors occurs via neurons with intermediately and slowly inactivating mechanocurrent. Such neurons contain the mechanically gated Piezo2 ion channel whose expression positively correlates with the expression of factors responsible for the development and function of mechanoreceptors. Conversely, Piezo2 expression negatively correlates with expression of molecules mediating the detection of temperature and pain, suggesting that the expansion of Piezo2-containing mechanoreceptors with prolonged mechanocurrent occurs at the expense of thermoreceptors and nociceptors. Our study suggests that the trade-off between neuronal subtypes is a general mechanism of tactile specialization at the level of somatosensory system. : Schneider et al. perform a cross-species analysis of somatosensory neurons from tactile specialist birds. The study reveals a trade-off in the expansion of Piezo2-containing neuronal touch receptors at the expense of temperature and pain receptors as part of a general mechanism that accompanies mechanosensory specialization. Keywords: Piezo2, Piezo1, sensory physiology, sensory adaptation, mechanosensitivity, mechanosensation, mechanoreceptor, somatosensitivity, touch, duck