To understand how behaviors arise in animals, it is necessary to investigate both the neural circuits and the biomechanics of the periphery. A tractable model system for studying multifunctional control is the feeding apparatus of the marine mollusk Aplysia californica. Previous in silico and in roboto models have investigated how the nervous and muscular systems interact in this system. However, these models are still limited in their ability to match in vivo data both qualitatively and quantitatively. We introduce a new neuromechanical model of Aplysia feeding that combines a modified version of a previously developed neural model with a novel biomechanical model that better reflects the anatomy and kinematics of Aplysia feeding. The model was calibrated using a combination of previously measured biomechanical parameters and hand-tuning to behavioral data. Using this model, simulated feeding experiments were conducted, and the resulting behavioral metrics were compared to animal data. The model successfully produces three key behaviors seen in Aplysia and demonstrates a good quantitative agreement with biting and swallowing behaviors. Additional work is needed to match rejection behavior quantitatively and to reflect qualitative observations related to the relative contributions of two key muscles, the hinge and I3. Future improvements will focus on incorporating the effects of deformable 3D structures in the simulated buccal mass.

Jumping is one of the most used forms of locomotion by insects, and a characteristic trait of the Orthoptera (locusts, crickets, and allies). Their specialized jumping behaviors have evolved for various functions, including travel, predator evasion, and flight initiation. While these jumping behaviors have been studied, targeted jumps required for navigating complex environments and hunting have received little attention. Here, we document a vertical jumping behavior in a species of neotropical predatory bush cricket (Phlugis cf. celerinicta. Tettigoniidae: Meconematinae), which uses visual cues to estimate target distance. Jumping kinematics were adjusted between jump heights (50mm, 75mm, and 100mm), with an increase in linear velocity and decrease in angular velocity at higher target heights. Body and leg postures also varied between jump heights. This study provides evidence that P. celerinicta can independently control both the speed at take-off and rotation rate based on target distance to achieve a precise and controlled landing.

Planthoppers are champion jumpers. Adult specimens are propelled by rapid movements of the hind legs, which can launch them a horizontal distance of 1.1 m with a take-off speed of 5.5 m/s, demonstrating high power output. The planthopper Issus Coleoptratus nymph achieves the precise synchronization required (30 μs) thanks to a pair of cuticular gears that kinematically link the hind legs. These cuticular gears show spectacular geometrical differences from conventional man-made mechanisms. We analysed the gear teeth of Issus Coleoptratus in combination with Micro-CT scans of the teeth to study the gearing properties. The results show that the Issus gear has a higher contact ratio than conventional man-made involute spur gears. If the Issus gear is rescaled to a tooth size equivalent to a conventional gear module of 4.5mm, an ISO standard involute gear can mesh, with no problem, with the Issus gears. In simulations, if the resized gear is subjected to the load borne by a conventional automotive gear made of steel, the maximum stress obtained for the Issus gear is higher on the tooth flank than for the conventional gear. This is a potentially interesting result, as one of the disadvantages of the ISO gear is that failure generally occurs at the root of the tooth due to stress concentration, leading to gear failure. Finally, a strength analysis is carried out with the application of the real load transmitted by the gear during a badly engaged jump showing that, thanks to its gear high contact ratio, it is possible for the Issus to compensate for any problems arising from a non-symmetrical jump, and therefore to perform a synchronized jump in any poorly engaged situation.

Studying the nervous system underlying animal motor control can shed light on how animals can adapt flexibly to a changing environment. We focus on the neural basis of feeding control in Aplysia californica. Using the Synthetic Nervous System framework, we developed a model of Aplysia feeding neural circuitry that balances neurophysiological plausibility and computational complexity. The circuitry includes neurons, synapses, and feedback pathways identified in existing literature. We organized the neurons into three layers and five subnetworks according to their functional roles. Simulation results demonstrate that the circuitry model can capture the intrinsic dynamics at neuronal and network levels. When combined with a simplified peripheral biomechanical model, it is sufficient to mediate three animal-like feeding behaviors (biting, swallowing, and rejection). The kinematic, dynamic, and neural responses of the model also share similar features with animal data. These results emphasize the functional roles of sensory feedback during feeding.

The mechanical forces experienced during movement and the time constants of muscle activation are important determinants of the durations of behaviors, which may both be affected by size-dependent scaling. The mechanics of slow movements in small animals are dominated by elastic forces and are thus quasistatic (i.e., always near mechanical equilibrium). Muscular forces producing movement and elastic forces resisting movement should both scale identically (proportional to mass⅔), leaving the scaling of the time constant of muscle activation to play a critical role in determining behavioral duration. We tested this hypothesis by measuring the duration of feeding behaviors in the marine mollusc Aplysia californica whose body sizes spanned three orders of magnitude. The duration of muscle activation was determined by measuring the time it took for muscles to produce maximum force as Aplysia attempted to feed on tethered inedible seaweed, which provided an in vivo approximation of an isometric contraction. The timing of muscle activation scaled with mass0.3. The total duration of biting behaviors scaled identically, with mass0.3, indicating a lack of additional mechanical effects. The duration of swallowing behavior, however, exhibited a shallower scaling of mass0.17. We suggest that this was due to the allometric growth of the anterior retractor muscle during development, as measured by micro computed tomography scans (microCT) of buccal masses. Consequently, larger Aplysia did not need to activate their muscles as fully to produce equivalent forces. These results indicate that muscle activation may be an important determinant of the scaling of behavioral durations in quasistatic systems.

Jaw morphology and function determine the range of dietary items that an organism can consume. Bite force is a function of the force exerted by the jaw musculature and applied via the skeleton. Bite force has been studied in a wide range of taxa using various methods, including direct measurement, or calculation from skulls or jaw musculature. Data for parrots (Psittaciformes), considered to have strong bites, are rare. This study calculated bite force for a range of parrot species of differing sizes using a novel method that relied on forces calculated using the area of jaw muscles measured in situ and their masses. The values for bite force were also recorded in vivo using force transducers, allowing for a validation of the dissection-based models. The analysis investigated allometric relationships between measures of body size and calculated bite force. Additionally, the study examined whether a measure of a muscle scar could be a useful proxy to estimate bite force in parrots. Bite force was positively allometric relative to body and skull mass, with macaws having the strongest bite recorded to date for a bird. Calculated values for bite force were not statistically different from measured values. Muscle scars from the adductor muscle attachment on the mandible can be used to accurately predict bite force in parrots. These results have implications for how parrots process hard food items and how bite forces are estimated in other taxa using morphological characteristics of the jaw musculature. Bite force in parrots has been explored using data from muscle masses. The values were validated by comparison with data for bite force collected from live parrots. The parrot's reputation for a strong bite force is well founded.image

Resilin, an elastomeric protein with remarkable physical properties that outperforms synthetic rubbers, is a near-ubiquitous feature of the power amplification mechanisms used by jumping insects. Catapult-like mechanisms, which incorporate elastic energy stores formed from a composite of stiff cuticle and resilin, are frequently used by insects to translate slow muscle contractions into rapid-release recoil movements. The precise role of resilin in these jumping mechanisms remains unclear, however. We used RNAi to reduce resilin deposition in the principal energy-storing springs of the desert locust ( Schistocerca gregaria ) before measuring jumping performance. Knockdown reduced the amount of resilin-associated fluorescence in the semilunar processes (SLPs) by 44% and reduced the cross-sectional area of the tendons of the hind leg extensor-tibiae muscle by 31%. This affected jumping in three ways: First, take-off velocity was reduced by 15% in knockdown animals, which could be explained by a change in the extrinsic stiffness of the extensor-tibiae tendon caused by the decrease in its cross-sectional area. Second, knockdown resulted in permanent breakages in the hind legs of 29% of knockdown locusts as tested by electrical stimulation of the extensor muscle, but none in controls. Third, knockdown locusts exhibited a greater decline in distance jumped when made to jump in rapid succession than did controls. We conclude that stiff cuticle acts as the principal elastic energy store for insect jumping, while resilin protects these more brittle structures against breakage from repeated use.

The coordination of complex behavior requires knowledge of both neural dynamics and the mechanics of the periphery. The feeding system of Aplysia californica is an excellent model for investigating questions in soft body systems’ neuromechanics because of its experimental tractability. Prior work has attempted to elucidate the mechanical properties of the periphery by using a Hill-type muscle model to characterize the force generation capabilities of the key protractor muscle responsible for moving Aplysia’s grasper anteriorly, the I2 muscle. However, the I1/I3 muscle, which is the main driver of retractions of Aplysia’s grasper, has not been characterized. Because of the importance of the musculature’s properties in generating functional behavior, understanding the properties of muscles like the I1/I3 complex may help to create more realistic simulations of the feeding behavior of Aplysia, which can aid in greater understanding of the neuromechanics of soft-bodied systems. To bridge this gap, in this work, the I1/I3 muscle complex was characterized using force-frequency, length-tension, and force-velocity experiments and showed that a Hill-type model can accurately predict its force-generation properties. Furthermore, the muscle’s peak isometric force and stiffness were found to exceed those of the I2 muscle, and these results were analyzed in the context of prior studies on the I1/I3 complex’s kinematics in vivo.

The passive dynamics of stance can explain why large animals, like horses and humans, require neuromuscular activity to maintain stance whereas smaller animals like cockroaches do not [20]. The dynamic properties that govern an animal's movement, like inertia, stiffness, and damping, are dictated by its size, scaling with its length [28]. The natural frequency of an animal's limb in stance can be predicted using its stiffness to inertia ratio, which scales inversely with length. We theorize that the passive mechanics of smaller animal limbs, with higher resonant frequencies than walking cycle frequencies, restore limb position quickly enough that neuromuscular intervention is not needed to correct perturbations during stance. Larger animals, however, require muscle activation since their mechanics depend more on inertia and are less dominated by viscoelastic effects, leading to a lower natural frequency.

There is increasing interest from evolutionary biologists in the evolution of avian bill shape, how the bill is used during feeding and, in particular, the bite forces the bill can deliver. Bite force exhibits isometry with the total mass of the jaw musculature, but there is variation in the functional categories of the jaw muscles in different avian taxa. Qualitative descriptions of the jaw musculature do not allow analysis of the relative contributions that adductor or retractor muscles play in generating a bite force. This study is a meta-analysis of published data for body mass and the mass of the jaw musculature in 66 bird species from 10 orders. The masses of the different muscles contributing to adduction and retraction in closing the jaw, and to depression and protraction in opening the jaw, were summed and allometric relationships explored before investigating the effects of taxonomic order on these relationships. The categories of muscles, and the masses of each category of jaw musculature varied among avian orders. Some species, such as the flightless ratites, had relatively small jaw muscle mass but parrots had an additional adductor muscle. Phylogenetically controlled relationships between body mass and the mass of each muscle category irrespective of taxonomic order were isometric. However, analysis of covariance revealed significant interactions between body mass and taxonomic order. Most orders had low values for body-mass-specific muscle masses in the jaw with the notable exceptions of the Passeriformes (songbirds) and Psittaciformes (parrots). The values of these orders were 3-4 times greater, although the relative amounts of muscles contributing to adduction and retraction were similar in Psittaciformes, but adduction was markedly higher in Passeriformes. The results of these analyses highlight the lack of species-specific data for most birds, which is adversely impacting our understanding of the anatomical features that are determining the functional properties of the bill during feeding.

Animals often leap from substrates that give way under them, such as leaves, soft ground or flexible branches. This provides an added complexity for latch-mediated spring-actuated (LaMSA) jumping animals because the spring-loaded system often works so quickly that neural feedback cannot adjust for errors caused by a yielding substrate. We studied a LaMSA jumper, the grasshopper, to determine how the mechanical properties of a substrate giving way under them would affect the kinematics of the jump. We measured this by allowing grasshoppers to leap from two diving boards, a long one that could generate a whole range of relative stiffnesses, and a shorter, much lighter, but stiffer board. Substrate stiffness was manipulated by then placing the grasshopper on different locations on that diving board, presenting from 30% of the grasshopper's leg stiffness to 200 times the grasshoppers leg stiffness. For platform stiffnesses that were less than that of the grasshopper, take-off velocity and kinetic energy were reduced, but jump elevation (the jump trajectory) was unaffected. For stiffnesses that were greater than that of the grasshopper, there was no effect on take-off velocity and kinetic energy. When jumping from an extremely light and stiff substrate, recoil of the surface allowed the grasshopper to recover some of the lost energy. Consequently, when jumping from substrates that are less stiff than they are (such as floppy leaves), grasshoppers must contend with lower take-off velocities, but jump direction is unaffected.

This paper discusses the design decisions, process, and results for a set of robotic rat hindlimbs scaled up to 2.5 times the size of the rat. The design is inspired by a previous model from within our lab, but includes a variety of improvements to further the utility and biological accuracy of the model. The robot is comprised of two legs with four motors each to actuate sagittal rotations of the hip, knee, and ankle joints as well as an internal hip rotation. The motor’s torque, inertial, viscous, and stiffness properties are characterized for dynamic scaling to be properly implemented in the future control scheme. With direct position commands, the robot’s joint movements are able to reflect those of the rat, proving its validity as a test bed for the implementation of future neural control schemes.

Locusts (Schistocerca gregaria) jump using a latch mediated spring actuated system in the femur-tibia joint of their metathoracic legs. These jumps are exceptionally fast and display angular rotation immediately after take-off. In this study, we focus on the angular velocity, at take-off, of locusts ranging between 0.049 and 1.50 g to determine if and how rotation-rate scales with size. From 263 jumps recorded from 44 individuals, we found that angular velocity scales with mass(-0.33), consistent with a hypothesis of locusts having a constant rotational kinetic energy density. Within the data from each locust, angular velocity increased proportionally with linear velocity, suggesting the two cannot be independently controlled and thus a fixed energy budget is formed at take-off. On average, the energy budget of a jump is distributed 98.7% to translational kinetic energy and gravitational potential energy, and 1.3% to rotational kinetic energy. The percentage of energy devoted to rotation was constant across all sizes of locusts and represents a very small proportion of the energy budget. This analysis suggests that smaller locusts find it harder to jump without body rotation.

Ultrafast movements propelled by springs and released by latches are thought limited to energetic adjustments prior to movement, and seemingly cannot adjust once movement begins. Even so, across the tree of life, ultrafast organisms navigate dynamic environments and generate a range of movements, suggesting unrecognized capabilities for control. We develop a framework of control pathways leveraging the non-linear dynamics of spring-propelled, latch-released systems. We analytically model spring dynamics and develop reduced-parameter models of latch dynamics to quantify how they can be tuned internally or through changing external environments. Using Lagrangian mechanics, we test feedforward and feedback control implementation via spring and latch dynamics. We establish through empirically-informed modeling that ultrafast movement can be controllably varied during latch release and spring propulsion. A deeper understanding of the interconnection between multiple control pathways, and the tunability of each control pathway, in ultrafast biomechanical systems presented here has the potential to expand the capabilities of synthetic ultra-fast systems and provides a new framework to understand the behaviors of fast organisms subject to perturbations and environmental non-idealities.

The Orthoptera are a diverse insect order well known for their locomotive capabilities. To jump, the bush-cricket uses a muscle actuated (MA) system in which leg extension is actuated by contraction of the femoral muscles of the hind legs. In comparison, the locust uses a latch mediated spring actuated (LaMSA) system, in which leg extension is actuated by the recoil of spring-like structure in the femur. The aim of this study was to describe the jumping kinematics of Mecopoda elongata (Tettigoniidae) and compare this to existing data in Schistocerca gregaria (Acrididae), to determine differences in control of rotation during take-off between similarly sized MA and LaMSA jumpers. 269 jumps from 67 individuals of M. elongata with masses from 0.014 g to 3.01 g were recorded with a high-speed camera setup. In M. elongata , linear velocity increased with mass 0.18 and the angular velocity (pitch) decreased with mass −0.13 . In S. gregaria , linear velocity is constant and angular velocity decreases with mass −0.24 . Despite these differences in velocity scaling, the ratio of translational kinetic energy to rotational kinetic energy was similar for both species. On average, the energy distribution of M. elongata was distributed 98.8% to translational kinetic energy and 1.2% to rotational kinetic energy, whilst in S. gregaria it is 98.7% and 1.3%, respectively. This energy distribution was independent of size for both species. Despite having two different jump actuation mechanisms, the ratio of translational and rotational kinetic energy formed during take-off is fixed across these distantly related orthopterans.

Abstract During behavior, the work done by actuators on the body can be resisted by the body's inertia, elastic forces, gravity, or viscosity. The dominant forces that resist actuation have major consequences on the control of that behavior. In the literature, features and actuation of locomotion, for example, have been successfully predicted by nondimensional numbers (e.g. Froude number and Reynolds number) that generally express the ratio between two of these forces (gravitational, inertial, elastic, and viscous). However, animals of different sizes or motions at different speeds may not share the same dominant forces within a behavior, making ratios of just two of these forces less useful. Thus, for a broad comparison of behavior across many orders of magnitude of limb length and cycle period, a dimensionless number that includes gravitational, inertial, elastic, and viscous forces is needed. This study proposes a nondimensional number that relates these four forces: the phase shift (ϕ) between the displacement of the limb and the actuator force that moves it. Using allometric scaling laws, ϕ for terrestrial walking is expressed as a function of the limb length and the cycle period at which the limb steps. Scale-dependent values of ϕ are used to explain and predict the electromyographic (EMG) patterns employed by different animals as they walk.

Robots that use impulsive mechanisms to achieve high-speed and high-powered motion are becoming more common and better understood, but control of these systems remains relatively rudimentary. Among robots that use spring actuation to generate motion, robot actuation and mechanisms are usually not controlled intentionally in order to achieve variation in the system's behavior, or they are controlled only roughly via adjustments made to the amount of energy stored in the mechanism. We describe the development, construction, and test of an impulsive catapult mechanism whose design is inspired by the grasshopper leg and for which extensive variation in the projectile trajectory is achieved by force control of the actuator that restrains the spring. As a step toward future controlled jumping robots, we give a detailed model of this system, validate this model experimentally, and explain how the actuator dynamics are critical to our ability to vary the system's trajectory using this approach. This work represents a novel approach to the control of spring actuated robots and illustrates how they can be controlled even under highly limiting actuator constraints.