Neuronal mechanism for acute mechanosensitivity in tactile-foraging waterfowl

Abstract

Relying almost exclusively on their acute sense of touch, tactileforaging 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 tactileforaging 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.A nimals with acute sense of touch provide an opportunity to study cellular and molecular principles of mechanoreception from an unconventional perspective (1, 2). Tactile-foraging waterfowl of the Anatidae family rely on their acute sense of touch rather than vision to find food. Using a complex array of highly coordinated feeding techniques-straining, pecking, and dabbling-they can selectively collect gastropods, worms, crustaceans, and plant matter even in murky water with high precision and efficiency. This highly discriminatory feeding behavior relies on the acquisition and rapid processing of sensory information coming from numerous mechanoreceptors in the bill (3).Mechanoreceptors are cell-neurite complexes that specialize in the detection of diverse mechanical stimuli. The most numerous mechanoreceptors in the bill skin of Anatidae birds are Herbst and Grandry corpuscles, which are present at high density (up to 150 receptors per square millimeter) 50-100 μm below the epidermis of dorsal and ventral surfaces of the upper and lower bill (4, 5). The mechanoreceptors are innervated by rapidly adapting primary afferents projecting from the trigeminal ganglia (TG) (Fig. 1A) and are best tuned to detect vibration and velocity (6-10). In this sense, Herbst and Grandry organs appear functionally homologous to the mammalian Pacinian and Meissner corpuscles, respectively. Following stimulus detection, mechanosensory information is processed in the trigeminal nucleus (PrV) of the brainstem. In tactile foragers, such as ducks, PrV accounts for a significantly larger fraction of total brain volume compared with visual foragers, such as chicken (11). This augmented neural representation reflects the need to process the complex and abundant tactile information from the primary afferents of the trigeminal nerve. However, even though the general layout of the mechanosensory system is well established, the contribution of primary afferents in stimulus detection is unclear.In rodents, over 80% of somatose...

Piezo Proteins: Regulators of Mechanosensation and Other Cellular Processes

“…The skin of the duck bill contains numerous mechanoreceptive end organs that are innervated by primary afferents from TG. The expansion of Piezo2-positive mechanoreceptors in duck TG, where these cells account for up to 85% of the neuronal population, further supports the notion of a key role for this protein in light touch perception (63).…”

“…Piezo2 activity has been linked to mechanosensitive neurons in DRG (4,15,20,60,61) and TG (62,63) Knockdown studies reveal that Piezo2 is responsible for a majority of the rapidly desensitizing MA current in murine DRG neurons. Piezo2-expressing neurons, however, do not seem to belong to a single functional subtype.…”

“…A recent study has revealed an unprecedented up-regulation of Piezo2-expressing large-diameter neurons in TG of acutely mechanosensitive species-tactile foraging ducks (63). The skin of the duck bill contains numerous mechanoreceptive end organs that are innervated by primary afferents from TG.…”

Cell Type Specific Splicing of Piezo2 Regulates Mechanotransduction

“…In mammals, other forms of mechanosensory specialization have been observed. For instance, sensory ganglia with different representations of mechanosensory neurons (Schneider et al, 2014) and signaling components (Gerhold et al, 2013) have been reported. This suggests that several strategies have been used to allow sensory specialization.…”

Evolutionary Specialization of Tactile Perception in Vertebrates

“…Finally, MA currents from dissociated duck TG neurons are larger in amplitude, are longer in duration, and require less stimulus intensity than the same group of neurons from mice. Overall, duck TG neurons are innately more mechanosensitive than mouse cells, providing an explanation to the exceptional mechanosensitivity of this species at the neuronal level (71). The majority of trigeminal neurons in several tactile-foraging duck subspecies are LTMRs expressing Piezo2 (71), a known mechanotransducer discovered in the somatosensory system of mice (15).…”