Sensing Force by Trigeminal Neurons of Acutely Mechanosensitive Birds

Mechanosensation is a fundamental way animals interact with the environment, but it remains the least well understood at cellular and molecular level. Somatosensory ganglia of the standard laboratory species house a highly diverse population of neurons, where low-threshold mechanoreceptors - the neurons that innervate light touch receptors in the skin - represent only a small fraction. This heterogeneity significantly impedes progress in understanding functional roles of somatosensory neurons in light touch perception. Here, we explored functional specialization of somatosensory ganglia from animals which have taken the sense of touch to the extreme - tactile foraging ducks. These animals have acutely mechanosensitive bill innervated by trigeminal (TG) neurons, and as such provide an opportunity to study general principles of mechanotransduction from an unconventional standpoint. We found that, in contrast to species without tactile specialization, the majority (85%) of duck TG neurons are large-diameter myelinated mechanoreceptors expressing the mechano-gated ion channel Piezo2. Electrophysiological analyses showed that mechanosensitivity of duck TG neurons has been optimized in three ways. Compared to mouse cells, duck neurons exhibit (i) lowered threshold of mechano-activation, (ii) elevated signal amplification gain, and (iii) prolonged kinetics of inactivation, all of which increase the amount of depolarizing charge entering the cell upon mechanical stimulation. Thus, duck TG neurons have augmented intrinsic ability to convert mechanical force into excitatory ionic current, which explains the acute mechanosensory properties of the duck bill. Our studies emphasize a key role of the intrinsic mechanosensory ability of somatosensory neurons in touch physiology, reveal an evolutionary strategy utilized by vertebrates to hone tactile perception, and suggest a novel model system to study the sense of touch at the cellular and molecular level.Schneider ER, Gracheva EO, Bagriantsev SN et al, PNAS 2014 (e-pub Sept 22).