Molecular basis of tactile specialization in the duck bill

Abstract

Tactile-foraging ducks are specialist birds known for their touch-dependent feeding behavior. They use dabbling, straining, and filtering to find edible matter in murky water, relying on the sense of touch in their bill. Here, we present the molecular characterization of embryonic duck bill, which we show contains a high density of mechanosensory corpuscles innervated by functional rapidly adapting trigeminal afferents. In contrast to chicken, a visually foraging bird, the majority of duck trigeminal neurons are mechanoreceptors that express the Piezo2 ion channel and produce slowly inactivating mechano-current before hatching. Furthermore, duck neurons have a significantly reduced mechano-activation threshold and elevated mechano-current amplitude. Cloning and electrophysiological characterization of duck Piezo2 in a heterologous expression system shows that duck Piezo2 is functionally similar to the mouse ortholog but with prolonged inactivation kinetics, particularly at positive potentials. Knockdown of Piezo2 in duck trigeminal neurons attenuates mechano current with intermediate and slow inactivation kinetics. This suggests that Piezo2 is capable of contributing to a larger range of mechano-activated currents in duck trigeminal ganglia than in mouse trigeminal ganglia. Our results provide insights into the molecular basis of mechanotransduction in a tactile-specialist vertebrate.

Piezo2 integrates mechanical and thermal cues in vertebrate mechanoreceptors

“…However, in contrast to other vertebrates, including rodents and visually foraging birds, duck TG contains an unusually high proportion of light touch receptors that develop at the expense of nociceptors and thermoreceptors. This results in mechanosensory specialization in the bill toward tactile foraging (33)(34)(35). The commonality between the potentiating effects of cold on MA current in mouse and duck somatosensory ganglia strongly suggests that the peripheral integration of thermal and mechanical cues is an evolutionarily conserved property of vertebrate mechanoreceptors.…”

“…MK905889). DRG neurons from 6-to 8-wk-old mice and TG neurons from embryonic day 22 to 24 duck embryos were acutely dissociated as previously described (34,35). Electrophysiological recordings of MA currents from neurons and cell lines were performed at different temperatures in the whole-cell mode in response to indentation with a glass probe (35,67,69).…”

“…To do this, we analyzed neurons from the TG of Pekin duck (Anas platyrhynchos domesticus), a tactile-specialist bird (15). The largest neuronal group in duck TG are Piezo2expressing low-threshold mechanoreceptors, which support the specialized tactile feeding apparatus in the bill (33)(34)(35). Like other vertebrates, the duck TG lacks proprioceptors.…”

Lamellar cells in Pacinian and Meissner corpuscles are touch sensors

“…To test whether lamellar cells play active role in the detection of touch, we developed a glabrous skin preparation from the bill of Pekin duck, a tactile specialist bird 7,17 . Duck bill skin contains a dense population of Pacinian and Meissner corpuscles, referred to as Herbst and Grandry corpuscles, respectively 18,19 . Like their mammalian counterparts, duck corpuscles are innervated by rapidly-adapting mechanoreceptors and are tuned to detect transient pressure and vibration [19][20][21][22] .…”

“…Duck bill skin contains a dense population of Pacinian and Meissner corpuscles, referred to as Herbst and Grandry corpuscles, respectively 18,19 . Like their mammalian counterparts, duck corpuscles are innervated by rapidly-adapting mechanoreceptors and are tuned to detect transient pressure and vibration [19][20][21][22] . Optical and electron microscopic analyses of an ex vivo preparation of duck bill skin ( Fig.…”