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Biological cellular structures have inspired many scientific disciplines to design synthetic structures that can mimic their functions. Here, we closely emulate biological cellular structures in a rationally designed synthetic multicellular hybrid ion pump, composed of hydrogen-bonded [EMIM + ][TFSI − ] ion pairs on the surface of silica microstructures (artificial mechanoreceptor cells) embedded into thermoplastic polyurethane elastomeric matrix (artificial extracellular matrix), to fabricate ionic mechanoreceptor skins. Ionic mechanoreceptors engage in hydrogen bond-triggered reversible pumping of ions under external stimulus. Our ionic mechanoreceptor skin is ultrasensitive (48.1–5.77 kPa −1 ) over a wide spectrum of pressures (0–135 kPa) at an ultra-low voltage (1 mV) and demonstrates the ability to surpass pressure-sensing capabilities of various natural skin mechanoreceptors (i.e., Merkel cells, Meissner’s corpuscles, Pacinian corpuscles). We demonstrate a wearable drone microcontroller by integrating our ionic skin sensor array and flexible printed circuit board, which can control directions and speed simultaneously and selectively in aerial drone flight. Wearable pressure sensors have a range of potential applications. Here, the authors develop ion pairs decorated silica microstructures embedded in an elastomeric matrix to mimic natural skin mechanoreceptors’ functions for applications in pressure-sensitive artificial skin.

Deploying a conserved mechanosensory neuron known as the concentric hair cell, cnidarians have evolved diverse mechanoreceptors from hydroid filiform tentacles to jellyfish statocysts. However, it is unknown whether cnidarian mechanoreceptor evolution has relied solely on repurposing a single ancestral mechanosensory neuron type. Here we report evidence for cell-type diversity of mechanosensory neurons in sea-anemone cnidarian Nematostella vectensis . Uncovered in the ectoderm of feeding tentacles are conventional type I hair cells and previously unrecognized type II hair cells differing in the structure of apical sensory apparatus and synapses. Moreover, we identify TRP channel-encoding gene polycystin-1 as a type-II-hair-cell-specific essential mediator of gentle touch response. Ontogenically, type I and type II hair cells derive from distinct postmitotic precursors that begin forming at different phases of larval development. Taken together, our findings suggest that anatomically, molecularly, and developmentally distinct mechanosensory neurons diversified within Cnidaria, or prior to the divergence of Cnidaria and Bilateria. Cnidarians have evolved an array of cell types, from mechanoreceptors to stinging cells. Here they provide evidence for a diversity of mechanosensory neural cell types in a sea anemone and reveal that evolutionary histories of animal mechanosensory neurons are more complex than previously recognized.

Collective behaviour in animal groups can improve individual perception and decision-making, but the neural mechanisms involved have been hard to access in classic models for these phenomena; here it is shown that Drosophila ’s olfactory responses are enhanced in groups of flies, through mechanosensory neuron-dependent touch interactions. How fruit-fly swarms stay in touch Schooling fish, flocking birds and human crowds can enhance the perception and decision-making of individuals in the group, but the neural mechanisms involved have been hard to determine. Richard Benton and colleagues use a more accessible model in which to study group behaviour: they show that weak odour-avoidance in individual fruitflies can be enhanced in groups of flies, thanks to cascades of appendage touch interactions between pairs of flies. By identifying the mechanosensory neurons and ion channels involved, the authors open the door to a neural-circuit dissection of collective behaviour in animal groups. Collective behaviour enhances environmental sensing and decision-making in groups of animals 1 , 2 . Experimental and theoretical investigations of schooling fish, flocking birds and human crowds have demonstrated that simple interactions between individuals can explain emergent group dynamics 3 , 4 . These findings indicate the existence of neural circuits that support distributed behaviours, but the molecular and cellular identities of relevant sensory pathways are unknown. Here we show that Drosophila melanogaster exhibits collective responses to an aversive odour: individual flies weakly avoid the stimulus, but groups show enhanced escape reactions. Using high-resolution behavioural tracking, computational simulations, genetic perturbations, neural silencing and optogenetic activation we demonstrate that this collective odour avoidance arises from cascades of appendage touch interactions between pairs of flies. Inter-fly touch sensing and collective behaviour require the activity of distal leg mechanosensory sensilla neurons and the mechanosensory channel NOMPC 5 , 6 . Remarkably, through these inter-fly encounters, wild-type flies can elicit avoidance behaviour in mutant animals that cannot sense the odour—a basic form of communication. Our data highlight the unexpected importance of social context in the sensory responses of a solitary species and open the door to a neural-circuit-level understanding of collective behaviour in animal groups.

Throughout vertebrates, cerebrospinal fluid-contacting neurons (CSF-cNs) are ciliated cells surrounding the central canal in the ventral spinal cord. Their contribution to modulate locomotion remains undetermined. Recently, we have shown CSF-cNs modulate locomotion by directly projecting onto the locomotor central pattern generators (CPGs), but the sensory modality these cells convey to spinal circuits and their relevance to innate locomotion remain elusive. Here, we demonstrate in vivo that CSF-cNs form an intraspinal mechanosensory organ that detects spinal bending. By performing calcium imaging in moving animals, we show that CSF-cNs respond to both passive and active bending of the spinal cord. In mutants for the channel Pkd2l1, CSF-cNs lose their response to bending and animals show a selective reduction of tail beat frequency, confirming the central role of this feedback loop for optimizing locomotion. Altogether, our study reveals that CSF-cNs constitute a mechanosensory organ operating during locomotion to modulate spinal CPGs. CSF-contacting neurons are known to project to locomotor CPGs although their relevance to active locomotion is unclear. Here, the authors show that these cells constitute a mechanosensory organ relying on PKD2L1 channels to detect spinal cord curvature and modulate locomotor frequency in freely moving animals.

A Drosophila chemosensory receptor, expressed in leg sensory neurons, is necessary for behavioural and molecular synchronization of the fly’s circadian clock to low-amplitude temperature cycles; this temperature-sensing pathway functions independently from the known temperature sensors of the fly’s antennae. Temperature rhythm sets the body clock The roughly 24-hour period of circadian clocks is largely independent of ambient temperature but the phase can be synchronized, in the absence of light variations, to the cycle of warmer (day) and colder (night) temperatures, with a sensitivity as fine as ±2° C. Now Ralf Stanewsky and colleagues identify the chemosensory receptor IR25a, expressed in internal stretch (chordotonal) sensory neurons in the leg of Drosophila , as necessary for both behavioural and molecular synchronization of the animal's circadian clock to low-amplitude temperature cycles. They further show that this new temperature-sensing pathway functions independently from the known temperature sensors of the fly's antennas. Circadian clocks are endogenous timers adjusting behaviour and physiology with the solar day 1 . Synchronized circadian clocks improve fitness 2 and are crucial for our physical and mental well-being 3 . Visual and non-visual photoreceptors are responsible for synchronizing circadian clocks to light 4 , 5 , but clock-resetting is also achieved by alternating day and night temperatures with only 2–4 °C difference 6 , 7 , 8 . This temperature sensitivity is remarkable considering that the circadian clock period (~24 h) is largely independent of surrounding ambient temperatures 1 , 8 . Here we show that Drosophila Ionotropic Receptor 25a (IR25a) is required for behavioural synchronization to low-amplitude temperature cycles. This channel is expressed in sensory neurons of internal stretch receptors previously implicated in temperature synchronization of the circadian clock 9 . IR25a is required for temperature-synchronized clock protein oscillations in subsets of central clock neurons. Extracellular leg nerve recordings reveal temperature- and IR25a-dependent sensory responses, and IR25a misexpression confers temperature-dependent firing of heterologous neurons. We propose that IR25a is part of an input pathway to the circadian clock that detects small temperature differences. This pathway operates in the absence of known ‘hot’ and ‘cold’ sensors in the Drosophila antenna 10 , 11 , revealing the existence of novel periphery-to-brain temperature signalling channels.

Sensory hair cells are mechanoreceptors required for hearing and balance functions. From embryonic development, hair cells acquire apical stereociliary bundles for mechanosensation, basolateral ion channels that shape receptor potential, and synaptic contacts for conveying information centrally. These key maturation steps are sequential and presumed coupled; however, whether hair cells emerging postnatally mature similarly is unknown. Here, we show that in vivo postnatally generated and regenerated hair cells in the utricle, a vestibular organ detecting linear acceleration, acquired some mature somatic features but hair bundles appeared nonfunctional and short. The utricle consists of two hair cell subtypes with distinct morphological, electrophysiological and synaptic features. In both the undamaged and damaged utricle, fate-mapping and electrophysiology experiments showed that Plp1+ supporting cells took on type II hair cell properties based on molecular markers, basolateral conductances and synaptic properties yet stereociliary bundles were absent, or small and nonfunctional. By contrast, Lgr5+ supporting cells regenerated hair cells with type I and II properties, representing a distinct hair cell precursor subtype. Lastly, direct physiological measurements showed that utricular function abolished by damage was partially regained during regeneration. Together, our data reveal a previously unrecognized aberrant maturation program for hair cells generated and regenerated postnatally and may have broad implications for inner ear regenerative therapies.

Differential coordination of growth and patterning across metazoans gives rise to a diversity of sizes and shapes at tissue, organ and organismal levels. Although tissue size and tissue function can be interdependent 1 – 5 , mechanisms that coordinate size and function remain poorly understood. Planarians are regenerative flatworms that bidirectionally scale their adult body size 6 , 7 and reproduce asexually, via transverse fission, in a size-dependent manner 8 – 10 . This model offers a robust context to address the gap in knowledge that underlies the link between size and function. Here, by generating an optimized planarian fission protocol in Schmidtea mediterranea , we show that progeny number and the frequency of fission initiation are correlated with parent size. Fission progeny size is fixed by previously unidentified mechanically vulnerable planes spaced at an absolute distance along the anterior–posterior axis. An RNA interference screen of genes for anterior–posterior patterning uncovered components of the TGFβ and Wnt signalling pathways as regulators of the frequency of fission initiation rather than the position of fission planes. Finally, inhibition of Wnt and TGFβ signalling during growth altered the patterning of mechanosensory neurons—a neural subpopulation that is distributed in accordance with worm size and modulates fission behaviour. Our study identifies a role for TGFβ and Wnt in regulating size-dependent behaviour, and uncovers an interdependence between patterning, growth and neurological function. A planarian fission protocol shows that the number of progeny and the frequency of fission initiation correlate with parent size, and TGFβ and Wnt signalling components are identified as regulators of fission behaviour.

The sense of touch relies on detection of mechanical stimuli by specialized mechanosensory neurons. The scarcity of molecular data has made it difficult to analyze development of mechanoreceptors and to define the basis of their diversity and function. We show that the transcription factor c-Maf/c-MAF is crucial for mechanosensory function in mice and humans. The development and function of several rapidly adapting mechanoreceptor types are disrupted in c-Maf mutant mice. In particular, Pacinian corpuscles, a type of mechanoreceptor specialized to detect high-frequency vibrations, are severely atrophied. In line with this, sensitivity to high-frequency vibration is reduced in humans carrying a dominant mutation in the c-MAF gene. Thus, our work identifies a key transcription factor specifying development and function of mechanoreceptors and their end organs.

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.

Tunicates, the sister group of vertebrates, possess a mechanoreceptor organ, the coronal organ, which is considered the best candidate to address the controversial issue of vertebrate hair cell evolution. The organ, located at the base of the oral siphon, controls the flow of seawater into the organism and can drive the “squirting” reaction, i.e., the rapid body muscle contraction used to eject dangerous particles during filtration. Coronal sensory cells are secondary mechanoreceptors and share morphological, developmental, and molecular traits with vertebrate hair cells. In the colonial tunicate Botryllus schlosseri, we described coronal organ differentiation during asexual development. Moreover, we showed that the ototoxic aminoglycoside gentamicin caused morphological and mechanosensorial impairment in coronal cells. Finally, fenofibrate had a strong protective effect on coronal sensory cells due to gentamicin-induced toxicity, as occurs in vertebrate hair cells. Our results reinforce the hypothesis of homology between vertebrate hair cells and tunicate coronal sensory cells.