Biologically – Plausible Load Feedback from Dynamically Scaled Robotic Model Insect Legs

Researchers have been studying the mechanisms underlying animal motor control for many years using computational models and biomimetic robots. Since testing some theories in animals can be challenging, this approach can enable unique contributions to the field. An example of a system that benefits from this modeling and robotics approach is the campaniform sensillum (CS), a kind of sensory organ used to detect the loads exerted on an insect\u27s legs. The CS on the leg are found in groups on high-stress areas of the exoskeleton and have a major influence on the adaptation of walking behavior. The challenge for studying these sensors is recording CS output from freely walking insects, which would show what the sensors detect during behavior. To address this difficulty, 3 dynamically scaled robotic models of the middle leg of the stick insect Carausius morosus (C. morosus) and the fly Drosophila melanogaster (D. melanogaster) were constructed. Two of the robotic legs model the C. morosus and are scaled to a stick insect at a ratio of 15:1 and 25:1. The robotic fly leg is scaled 400:1 to the leg of the D. melanogaster. Strain gauges are affixed to locations and orientations that are analogous to those of major CS groups. The legs were attached to a linear guide to simulate weight and they stepped on a treadmill to mimic walking. Using these robotic models, it is possible to shed light on how the nervous system of insects detects load feedback, examine the effect of different tarsi designs on load feedback, and compare the CS measurement capabilities of different insects. As mentioned earlier, robotic legs allow for any experiment to be conducted, and strain data can still be recorded, unlike animals. I subjected the 15:1 stick leg to a range of stepping conditions, including various static loading, transient loading, and leg slipping. I then processed the strain data through a previously published dynamic computational model of CS discharge. This demonstrated that the CS signal can robustly signal increasing forces at the beginning of the stance phase and decreasing forces at the end of the stance phase or when the foot slips. The same model leg can then be further expanded upon, allowing us to test how different tarsus designs affect load feedback. To isolate various morphological effects, these tarsi were developed with differing degrees of compliance, passive grip, and biomimetic structure. These experiments demonstrated that the tarsus plays a distinct role in loading the leg because of the various effects each design had on the strain. In the final experiment, two morphologically distinct insects with homologous CS groups were compared. The 400:1 robotic fly middle leg and the 25:1 robotic stick insect middle leg were used for these tests. The measured strains were notably influenced by the leg morphology, stepping kinematics, and sensor locations. Additionally, the sensor locations were lacking in one species in comparison to the other measured strains that were already being measured by the present sensors. These findings contributed to the understanding of load sensing in animal locomotion, effects of tarsal morphology, and sensory organ morphology in motor control

Dynamik und Kinematik der Lokomotion von Formica polyctena

In der vorliegenden Dissertation wurde untersucht, welche kinematischen und dynamischen Muster sich bei der Ameisenlokomotion identifizieren lassen und wie sich diese im Vergleich zu größeren Arten darstellen. Es wurde gezeigt, dass Waldameisen bei ebener Lokomotion dieselbe Gangdynamik über einen weiten Geschwindigkeitsbereich benutzten, ohne das alternierende, tripodale Schrittmuster aufzulösen. Mit wachsenden Laufgeschwindigkeiten erhöhte sich Schrittlänge und Schrittfrequenz. Die Energetik des Körperschwerpunkts indizierte einen federnden Gang, da kinetische und potentielle Energie nahezu in Phase verliefen. In den Vorderbeinen wurde eine hohe Maß an Nachgiebigkeit festgestellt, welche zu geringen vertikalen Oszillationen des Körperschwerpunktes führt und die Aufrechterhaltung des Bodenkontaktes auch bei höheren Geschwindigkeiten ermöglicht. Federnde Gangarten, ohne Flugphasen, scheinen eine weit verbreitete Strategie bei kleinen, schnell laufenden Lebewesen zu sein und können hinlänglich gut über das bipedale Masse-Feder-Modell beschrieben werden. Diese Form der Lokomotion wird auch als „Grounded Running“ bezeichnet und scheint, gemäß unseren Ergebnissen, auch für Ameisen die bevorzugte Fortbewegungsstrategie in der Ebene zu sein. Grundvoraussetzung für das Gelingen des Projektes war die Entwicklung eines miniaturisierten Messplatzes zur Erfassung der dreidimensionalen Bodenreaktionskräfte der Einzelbeine kleiner Insekten, bei gleichzeitiger Aufzeichnung der Kinematik. Im Rahmen dieser Arbeit ist es gelungen eine neuartige Ultraminiaturkraftmessplattform mit einem Auflösungsvermögen im Mikronewton-Bereich zu entwickeln und gemeinsam mit einer Hochgeschwindigkeits-Videokamera in einen weltweit einzigartigen Messplatz zu integrieren

Kinetic energy fluctuation-driven locomotor transitions on potential energy landscapes of beam obstacle traversal and self-righting

Despite contending with constraints imposed by the environment, morphology, and physiology, animals move well by physically interactingwith the environment to use and transition between modes such as running, climbing, and self-righting. By contrast, robots struggle to do so in real world. Understanding the principles of how locomotor transitions emerge from constrained physical interaction is necessary for robots to move robustly using similar strategies. Recent studies discovered that discoid cockroaches use and transition between diverse locomotor modes to traverse beams and self-right on ground. For both systems, animals probabilistically transitioned between modes via multiple pathways, while its self-propulsion created kinetic energy fluctuation. Here, we seek mechanistic explanations for these observations by adopting a physics-based approach that integrates biological and robotic studies. We discovered that animal and robot locomotor transitions during beam obstacle traversal and ground self-righting are barrier-crossing transitions on potential energy landscapes. Whereas animals and robot traversed stiff beams by rolling their body betweenbeam, they pushed across flimsy beams, suggesting a concept of terradynamic favorability where modes with easier physical interaction are more likely to occur. Robotic beam traversal revealed that, system state either remains in a favorable mode or transitions to one when energy fluctuation is comparable to the transition barrier. Robotic self-righting transitions occurred similarly and revealed that changing system parameters lowers barriers over which comparable fluctuation can induce transitions. Thetransitionsof animalsin both systems mostly occurred similarly, but sensory feedback may facilitate its beam traversal. Finally, we developed a method to measure animal movement across large spatiotemporal scales in a terrain treadmill.Comment: arXiv admin note: substantial text overlap with arXiv:2006.1271

Adaptive load feedback robustly signals force dynamics in robotic model of Carausius morosus stepping

Animals utilize a number of neuronal systems to produce locomotion. One type of sensory organ that contributes in insects is the campaniform sensillum (CS) that measures the load on their legs. Groups of the receptors are found on high stress regions of the leg exoskeleton and they have significant effects in adapting walking behavior. Recording from these sensors in freely moving animals is limited by technical constraints. To better understand the load feedback signaled by CS to the nervous system, we have constructed a dynamically scaled robotic model of the Carausius morosus stick insect middle leg. The leg steps on a treadmill and supports weight during stance to simulate body weight. Strain gauges were mounted in the same positions and orientations as four key CS groups (Groups 3, 4, 6B, and 6A). Continuous data from the strain gauges were processed through a previously published dynamic computational model of CS discharge. Our experiments suggest that under different stepping conditions (e.g., changing “body” weight, phasic load stimuli, slipping foot), the CS sensory discharge robustly signals increases in force, such as at the beginning of stance, and decreases in force, such as at the end of stance or when the foot slips. Such signals would be crucial for an insect or robot to maintain intra- and inter-leg coordination while walking over extreme terrain

Application of Confocal Microscopy To Study the Neural Mechanisms Underlying Insect and Rodent Behavior

Posture and walking require support of the body weight, which is thought to be detected by sensory receptors in the legs. Specificity in sensory encoding occurs through the morphological properties of the sense organs (numerical distribution, receptor size) and their physiological response characteristics. These studies focus upon campaniform sensilla, receptors that detect forces as strains in the insect exoskeleton. To study the morphology of campaniform sensilla, the sites of mechanotransduction (cuticular caps) were imaged by light and confocal microscopy in four species (stick insects, cockroaches, blow flies and Drosophila). These data indicate that the gradient (range) of cap sizes may most closely correlate with the body weight. These studies support the idea that morphological properties of force-detecting sensory receptors in the legs may be tuned to reflect the body weight. Overall, this study indicates that the morphological properties of the sense organs are specifically tuned to provide information needed for postural stability and successful locomotion

Characterisation of the biomechanical, passive, and active properties of femur-tibia joint leg muscles in the stick insect Carausius morosus

The understanding of locomotive behaviour of an animal necessitates the knowledge not only about its neural activity but also about the transformation of this activity patterns into muscle activity. The stick insect is a well studied system with respect to its motor output which is shaped by the interplay between sensory signals, the central neural networks for each leg joint and the coordination between the legs. The muscles of the FT (femur-tibia) joint are described in their morphologies and their motoneuronal innervation patterns, however little is known about how motoneuronal stimulation affects their force development and shortening behaviour. One of the two muscles moving the joint is the extensor tibiae, which is particularly suitable for such an investigation as it features only three motoneurons that can be activated simultaneously, which comes close to a physiologically occuring activation pattern. Its antagonist, the flexor tibiae, has a more complex innervation and a biomechanical investigation is only reasonable at full motoneuronal recruitment. Muscle force and length changes were measured using a dual-mode lever system that was connected to the cut muscle tendon. Both tibial muscles of all legs were studied in terms of their geometry: extensor tibiae muscle length changes with the cosine of the FT joint angle, while flexor tibiae length changes with the negative cosine, except for extreme angles (close to 30° and 180°). For all three legs, effective flexor tibiae moment arm length (0.564 mm) is twice that of the extensor tibiae (0.282 mm). Flexor tibiae fibres are 1.5 times longer (2.11 mm) than extensor tibiae fibres (1.41 mm). Active isometric force measurements demonstrated that extensor tibiae single twitch force is notably smaller than its maximal tetanical force at 200 Hz (2-6 mN compared to 100-190 mN) and takes a long time to decrease completely (> 140 ms). Increasing either frequency or duration of the stimulation extends maximal force production and prolongs the relaxation time of the extensor tibiae. The muscle reveals `latch´ properties in response to a short-term increase in activation. Its working range is on the ascending limb of the force-length relationship (see Gordon et al. (1966b)) with a shift in maximum force development towards longer fibre lengths at lower activation. The passive static force increases exponentially with increasing stretch. Maximum forces of 5 mN for the extensor, and 15 mN for the flexor tibiae occur within the muscles´ working ranges. The combined passive torques of both muscles determine the rest position of the joint without any muscle activity. Dynamically generated forces of both muscles can become as large as 50-70 mN when stretch ramps mimick a fast middle leg swing phase. FT joint torques alone (with ablated muscles) do not depend on FT joint angle, but on deflection amplitude and velocity. Isotonic force experiments using physiological activation patterns demonstrate that the extensor tibiae acts like a low-pass filter by contracting smoothly to fast instantaneous stimulation frequency changes. Hill hyperbolas at 200 Hz vary a great deal with respect to maximal force (P0) but much less in terms of contraction velocity (V0) for both tibial muscles. Maximally stimulated flexor tibiae muscles are on average 2.7 times stronger than extensor tibiae muscles (415 mN and 151 mN), but contract only 1.4 times faster (6.05 mm/s and 4.39 mm/s). The dependence of extensor tibiae V0 and P0 on stimulation frequency can be described with an exponential saturation curve. V0 increases linearly with length within the muscle´s working range. Loaded release experiments characterise extensor and flexor tibiae series elastic components as quadratic springs. The mean spring constant of the flexor tibiae is 1.6 times larger than of the extensor tibiae at maximal stimulation. Extensor tibiae stretch and relaxation ramps show that muscle relaxation time constant slowly changes with muscle length, and thus muscle dynamics have a long-lasting dependence on muscle length history. High-speed video recordings show that changes in tibial movement dynamics match extensor tibiae relaxation changes at increasing stimulation duration

Passive Variable Compliance for Dynamic Legged Robots

Recent developments in legged robotics have found that constant stiffness passive compliant legs are an effective mechanism for enabling dynamic locomotion. In spite of its success, one of the limitations of this approach is reduced adaptability. The final leg mechanism usually performs optimally for a small range of conditions such as the desired speed, payload, and terrain. For many situations in which a small locomotion system experiences a change in any of these conditions, it is desirable to have a tunable stiffness leg for effective gait control. To date, the mechanical complexities of designing usefully robust tunable passive compliance into legs has precluded their implementation on practical running robots. In this thesis we present an overview of tunable stiffness legs, and introduce a simple leg model that captures the spatial compliance of our tunable leg. We present experimental evidence supporting the advantages of tunable stiffness legs, and implement what we believe is the first autonomous dynamic legged robot capable of automatic leg stiffness adjustment. Finally we discuss design objectives, material considerations, and manufacturing methods that lead to robust passive compliant legs

Multimodal Proprioceptive Integration in Sensorimotor Networks of an Insect Leg

An animal’s nervous system monitors the actions of the body using its sense of proprioception. This information is used for precise motor control and to enable coordinated interaction with the animal’s surroundings. Proprioception is a multimodal sense that includes feedback about limb movement and loading from various peripheral sense organs. The sensory information from distinct sense organs must be integrated by the network to form a coherent representation of the current proprioceptive state and to elicit appropriate motor behavior. By combining intra- and extracellular electrophysiological recording techniques with precise mechanical sensory stimulation paradigms, I studied multimodal proprioceptive integration in the sensorimotor network of the stick insect leg. The findings demonstrate where, when, and how sensory feedback from load-sensing campaniform sensilla (CS) is integrated with movement information from the femoral chordotonal organ (fCO) in the sensorimotor network controlling movement of the femur-tibia (FTi) joint. Proprioceptive information about distinct sensory modalities (load / movement) and from distinct sense organs of the same sensory modality (trochanterofemoral CS (tr/fCS) / tibial CS (tiCS)) was distributed into one network of local premotor nonspiking interneurons (NSIs). The NSIs’ processing of fCO, tr/fCS, and tiCS was antagonistic with respect to a given NSI’s effect on the motor output of extensor tibiae motor neurons (ExtTi MNs). Spatial summation of load and movement feedback occurred in the network of premotor NSIs, whereas temporal summation was shifted between sensory modalities. Load feedback (tr/fCS / tiCS) was consistently delayed relative to movement signals (fCO) throughout the sensorimotor pathways of sensory afferents, premotor NSIs, and ExtTi MNs. The connectivity between these neuron types was inferred using transmission times and followed distinct patterns for individual sense organs. At the motor output level of the system, the temporal shift of simultaneously elicited load and movement feedback caused load responses to be superimposed onto ongoing movement responses. These results raised the hypothesis that load could alter movement signal processing. Load (tiCS) affected movement (fCO) signal gain by presynaptic afferent inhibition. In postsynaptic premotor NSIs, this led to altered movement parameter dependence and nonlinear summation of load and movement signals. Specifically, the amplitude dependence of NSIs opposing ExtTi MN output was increased, and, consistently, the movement response gain of the slow ExtTi MN was decreased. Movement signal processing in the premotor network was altered depending on the proprioceptive context, i.e. the presence or absence of load feedback. Lateral presynaptic interactions between load (tiCS) and movement (fCO) afferents were reciprocal, i.e. existed from fCO to tiCS afferents and vice versa, and also occurred between sensory afferents of the same sense organ. Additionally, a new type of presynaptic interaction was identified. Load signals increased the gain of directional movement information by releasing unidirectionally velocity- or acceleration-sensitive fCO afferents from tonic presynaptic inhibition. Paired double recordings showed lateral connectivity also at the level of the premotor NSI network. NSIs interacted via reciprocal excitatory connections. Additionally, the activity of individual NSIs was correlated in the absence of external stimuli, and specific types of NSIs showed rhythmic 30 Hz oscillations of the resting membrane potential, indicating an underlying mechanism of network synchronization. Taken together, the results of this dissertation provide an understanding of the integration of multimodal proprioceptive feedback in the sensorimotor network by identifying neuronal pathways and mechanism underlying spatial and temporal signal summation. The local network uses multimodal signal integration for context-dependent sensory processing, thereby providing insights into the mechanism by which a local network can adapt sensory processing to the behavioral context. Initial results clearly highlight the necessity to consider lateral connections along sensorimotor pathways to unravel the complex computations underlying proprioceptive processing and motor control. The findings on the integration of proprioceptive signals, obtained in the resting animal, broaden our understanding of sensorimotor processing and motor control not only in the stationary, but also in the walking animal

Material, acoustic, and mechanical properties of mosquito and midge antennae

The aim of this PhD is to contribute to the understanding of antennal hearing in insects. To this end, Confocal Laser Scanning Microscopy (CLSM), Finite Element Modelling (FEM) and Laser Doppler Vibrometry (LDV) were employed. The combination of the first two allows, in absence of prior knowledge of the material properties of mosquito or midge antennae, to assess the material structure and to gauge which impact this distribution can have on the antenna's mechanical behaviour in response to sound. It was revealed that, rather than a simple beam of uniform cuticle, the antennae of the insects studied had patterns and distributions of hard and soft ring elements along the length of their antennae. These properties were simulated with FEM and showed that they can strongly influence the resonant frequency of the antennae. Further investigations were done on the vibrational behaviour of these insects with LDV. The males of T. brevipalpis, An. arabiensis and An. gambiae demonstrated strong self-oscillation with high Q-factors. Unlike the mosquitoes, vibrometry of C. riparius showed no relevant self-oscillation of the antenna. Female T. brevipalpis produced self-oscillation but weaker than the male. The three-dimensional pattern of self-oscillation in all investigated mosquito species follows a distorted elliptical path. When stimulated with sound, the self-oscillating antennae exhibited classic nonlinear behaviour such as entrainment and down-modulation. Taken together, this thesis highlights the complex mechanics of acoustic reception in mosquitoes and midges, both mechanically and structurally.The aim of this PhD is to contribute to the understanding of antennal hearing in insects. To this end, Confocal Laser Scanning Microscopy (CLSM), Finite Element Modelling (FEM) and Laser Doppler Vibrometry (LDV) were employed. The combination of the first two allows, in absence of prior knowledge of the material properties of mosquito or midge antennae, to assess the material structure and to gauge which impact this distribution can have on the antenna's mechanical behaviour in response to sound. It was revealed that, rather than a simple beam of uniform cuticle, the antennae of the insects studied had patterns and distributions of hard and soft ring elements along the length of their antennae. These properties were simulated with FEM and showed that they can strongly influence the resonant frequency of the antennae. Further investigations were done on the vibrational behaviour of these insects with LDV. The males of T. brevipalpis, An. arabiensis and An. gambiae demonstrated strong self-oscillation with high Q-factors. Unlike the mosquitoes, vibrometry of C. riparius showed no relevant self-oscillation of the antenna. Female T. brevipalpis produced self-oscillation but weaker than the male. The three-dimensional pattern of self-oscillation in all investigated mosquito species follows a distorted elliptical path. When stimulated with sound, the self-oscillating antennae exhibited classic nonlinear behaviour such as entrainment and down-modulation. Taken together, this thesis highlights the complex mechanics of acoustic reception in mosquitoes and midges, both mechanically and structurally