Wing structure and neural encoding jointly determine sensing strategies in insect flight

Weber, Alison I.; Daniel, Thomas L.; Brunton, Bingni W.

doi:10.1101/2021.02.09.430476

Cited by 3 publications

(1 citation statement)

References 78 publications

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“…Over the past two decades, research into embodied computation has relaxed this conceptual distinction by showing that computational tasks can be outsourced to the dynamics [6] and configuration of the compliant body [3,4], generating significant excitement about the role of softmaterials in robotics [7]. In organismic biology -this conceptual foundation has had important implications on our understanding of animal behavior [8][9][10].…”

Section: Introductionmentioning

confidence: 99%

Excitable mechanics embodied in a walking cilium

Bull¹,

Kroo²,

Prakash³

2021

Preprint

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Rapid transduction of sensory stimulation to action is essential for an animal to survive. To this end, most animals use the sub-second excitable and multistable dynamics of a neuromuscular system. Here, studying an animal without neurons or muscles, we report analogous excitable and multistable dynamics embedded in the physics of a 'walking' cilium. We define a 'walking cilium' as a phenomena where the locomotive force is generated through contact with a substrate which is periodically reset by steps in the direction of motion. We begin by showing that cilia can walk without specialized gait control and identify the characteristic scales of spatiotemporal height fluctuations of the tissue. With the addition of surface interaction, we construct a low-order dynamical model of this single-cilium sub-unit. In addition to studying the dynamics of a single cilium in isolation, we subsequently examine collections of these walking cilia. En route to an emergent model for ciliary walking, we demonstrate the limits of substrate mediated synchronization between cilia. In the desynchronized limit, our model shows evidence of localized multi-stability mediated by the crosstalk between locomotive forcing and height. The out-of-equilibrium mechanics -which govern this emergent excitable bistability -directly control the locomotive forcing of a walking cilia. This direct coupling bypasses the role of the synaptic junctions between neurons and muscles. We show a minimal mechanism -trigger waves -by which these walking cells may work together to achieve organism-scale collaboration, such as coordination of hunting strikes across 10 5 cells without central control.Significance: Eukaryotic cilia are both sensors and actuators. There is a growing field of research dedicated to understanding how stimulus is transformed into action through biochemical queues within these intricate sub-cellular structures. Here, we complement this ongoing research program by considering the hypothesis that these biochemical dynamics could be outsourced to the fast timescale response of the mechanics of an oscillating cilium. To accomplish this we studied how an emerging model organism with no muscles or neurons in the phylum placozoa (plate animals) move around using ciliary "walking". To our surprise, we found that ciliary walking can be effectively described as an excitable dynamical system. We expect that these results will enrich the discussion of how cilia can be used to coordinate the behavior of many cells without a governing neuromuscular system.

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Section: Introductionmentioning

confidence: 99%

Excitable mechanics embodied in a walking cilium

Bull¹,

Kroo²,

Prakash³

2021

Preprint

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Bio‐Inspired Large‐Area Soft Sensing Skins to Measure UAV Wing Deformation in Flight

Shin

Ott

Beuken

et al. 2021

Adv Funct Materials

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Biological organisms demonstrate remarkable agility in complex environments, especially in comparison to engineered robotic systems. In part, this is due to an organism's ability to detect disturbances and react to them quickly. To address the challenge of quickly sensing these same disturbances in robotic systems, this study proposes and demonstrates large‐area soft sensing skins designed to sense disturbances on unmanned aerial vehicles (UAVs) in flight. These skins are enabled by high‐resolution soft strain sensors embedded into a large‐area skin through a modular molding process that spans feature sizes from tens of microns to 0.675 m. The electronics of the sensing system enable the soft skins to be sampled fast enough to capture dynamic loads on a wing. Overall, the large‐area soft sensing skin demonstrates high sensitivity, mechanical robustness, and consistent sensor readings across static and dynamic tests. The use of the soft sensing skin during UAV flight demonstrates that the sensing skin can capture relevant flight dynamics on small UAVs. These results pave the way to large‐area soft sensing skins for fast and robust control of a wide variety of robotic systems.

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Intraspecific variation in the placement of campaniform sensilla on the wings of the hawkmothManduca sexta

Stanchak,

Deora,

Weber

et al. 2023

Preprint

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Flight control requires active sensory feedback, and insects have many sensors that help them estimate their current locomotor state, including campaniform sensilla, which are mechanoreceptors that sense strain resulting from deformation of the cuticle. Campaniform sensilla on the wing detect bending and torsional forces encountered during flight, providing input to the flight feedback control system. During flight, wings experience complex spatio-temporal strain patterns. Because campaniform sensilla detect only local strain, their placement on the wing is presumably critical for determining the overall representation of wing deformation; however, how these sensilla are distributed across wings is largely unknown. Here, we test the hypothesis that campaniform sensilla are found in stereotyped locations across individuals ofManduca sexta, a hawkmoth. We found that although campaniform sensilla are consistently found on the same veins or in the same regions of the wings, their total number and distribution can vary extensively. This suggests that there is some robustness to variation in sensory feedback in the insect flight control system. The regions where campaniform sensilla are consistently found provide clues to their functional roles, although some patterns might be reflective of developmental processes. Collectively, our results on intraspecific variation in campaniform sensilla placement on insect wings will help reshape our thinking on the utility of mechanosensory feedback for insect flight control and guide further experimental and comparative studies.

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Wing structure and neural encoding jointly determine sensing strategies in insect flight

Cited by 3 publications

References 78 publications

Excitable mechanics embodied in a walking cilium

Excitable mechanics embodied in a walking cilium

Bio‐Inspired Large‐Area Soft Sensing Skins to Measure UAV Wing Deformation in Flight

Intraspecific variation in the placement of campaniform sensilla on the wings of the hawkmothManduca sexta

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