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Because soft animals are deformable, their locomotion is particularly affected by external forces and they are expected to face challenges controlling movements in different environments and orientations.We have used the caterpillar Manduca sexta to study neuromechanical strategies of soft-bodied scansorial locomotion. Manduca locomotion critically depends on the timing of proleg grip release, which is mediated by the principal planta retractor muscle and its single motoneuron, PPR. During upright crawling, PPR firing frequency increases approximately 0.6 s before grip release but during upsidedown crawling, this activity begins significantly earlier, possibly pretensioning the muscle. Under different loading conditions the timing of PPR activity changes relative to the stance/swing cycle. PPR motor activity is greater during upside-down crawling but these frequency changes are too small to produce significant differences in muscle force. Detailed observation of the proleg tip show that it swells before the retractor muscle is activated. This small movement is correlated with the activation of more posterior body segments, suggesting that it results from indirect mechanical effects. The timing and direction of this proleg displacement implies that proleg grip release is a dynamic interplay of mechanics and active neural control. [ABSTRACT FROM AUTHOR]

Animals that must transition from horizontal to inclined or vertical surfaces typically change their locomotion strategy to compensate for the relative shift in gravitational forces. The species that have been studied have stiff articulated skeletons that allow them to redistribute ground reaction forces (GRFs) to control traction. Most also change their stepping patterns to maintain stability as they climb. In contrast, caterpillars, most of which are highly scansorial, soft-bodied, and lack rigid support or joints, can move with the same general kinematics in all orientations. In this study, we measure the GRFs exerted by the abdominal prolegs of Manduca sexta (Linnaeus) during locomotion. We show that, despite the orthogonal shift in gravitational forces, caterpillars use the same tension-based environmental skeleton strategy to crawl horizontally and to climb vertically. Furthermore, the transition from horizontal to vertical surfaces does not seem to require a change in gait; instead gravitational loading is used to help maintain a stancephase body tension against which the muscles can pull the body upwards. [ABSTRACT FROM AUTHOR]

Aimed movements require that an animal accurately locates the target and correctly reaches that location. One such behavior is the defensive strike seen in Manduca sexta larva. These caterpillars respond to noxious mechanical stimuli applied to their abdomen with a strike of the mandibles towards the location of the stimulus. The accuracy with which the first strike movement reaches the stimulus site depends on the location of the stimulus. Reponses to dorsal stimuli are less accurate than those to ventral stimuli and the mandibles generally land ventral to the stimulus site. Responses to stimuli applied to anterior abdominal segments are less accurate than responses to stimuli applied to more posterior segments and the mandibles generally land posterior to the stimulus site. A trade-off between duration of the strike and radial accuracy is only seen in the anterior stimulus location (body segment A4). The lower accuracy of the responses to anterior and dorsal stimuli can be explained by the morphology of the animal; to reach these areas the caterpillar needs to move its body into a tight curve. Nevertheless, the accuracy is not exact in locations that the animal has shown it can reach, which suggests that consistently aiming more ventral and posterior of the stimulation site might be a defense strategy. [ABSTRACT FROM AUTHOR]

Caterpillars can increase their body mass 10,000-fold in 2weeks. It is therefore remarkable that most caterpillars appear to maintain the same locomotion kinematics throughout their entire larval stage. This study examined how the body properties of a caterpillar might change to accommodate such dramatic changes in body load. Using Manduca sexta as a model system, we measured changes in body volume, tissue density and baseline body pressure, and the dimensions of load-bearing tissues (the cuticle and muscles) over a body mass range from milligrams to several grams. All Manduca biometrics relevant to the hydrostatic skeleton scaled allometrically but close to the isometric predictions. Body density and pressure were almost constant. We next investigated the effects of scaling on the bending stiffness of the caterpillar hydrostatic skeleton. The anisotropic non- linear mechanical response of Manduca muscles and soft cuticle has previously been quantified and modeled with constitutive equations. Using biometric data and these material laws, we constructed finite element models to simulate a hydrostatic skeleton under different conditions. The results show that increasing the internal pressure leads to a non-linear increase in bending stiffness. Increasing the body size results in a decrease in the normalized bending stiffness. Muscle activation can double this stiffness in the physiological pressure range, but thickening the cuticle or increasing the muscle area reduces the structural stiffness. These non-linear effects may dictate the effectiveness of a hydrostatic skeleton at different sizes. Given the shared anatomy and size variation in Lepidoptera larvae, these mechanical scaling constraints may implicate the diverse locomotion strategies in different species. [ABSTRACT FROM AUTHOR]

Animal locomotion is produced by co-coordinated patterns of motor activity that are generally organized by central pattern generators and modified by sensory feedback. Animals with remote sensing can anticipate obstacles and make adjustments in their gait to accommodate them. It is largely unknown how animals that rely on touch might use such information to adjust their gait. One possibility is immediate (reflexive) change in motor activity. Elongated animals, however, might modulate movements by passing information from anterior to posterior segments. Using the caterpillar Manduca sexta we examined the movements of the most anterior abdominal prolegs as they approached an obstacle. The first pair of prolegs anticipated the obstacle by lifting more quickly in the earliest part of the swing phase: the caterpillar had information about the obstacle at proleg lift-off. Sometimes the prolegs corrected their trajectory mid-step. Removal of sensory hairs on the stepping leg did not affect the early anticipatory movements, but did change the distance at which the mid-step corrections occurred. We conclude that anterior sensory information can be passed backwards and used to modulate an ongoing crawl. The local sensory hairs on each body segment can then fine-tune movements of the prolegs as they approach an obstacle. [ABSTRACT FROM AUTHOR]

The measurement of forces generated during locomotion is essential for the development of accurate mechanical models of animal movements. However, animals that lack a stiff skeleton tend to dissipate locomotor forces in large tissue deformation and most have complex or poorly defined substrate contacts. Under these conditions, measuring propulsive and supportive forces is very difficult. One group that is an exception to this problem is lepidopteran larvae which, despite lacking a rigid skeleton, have well-developed limbs (the prolegs) that can be used for climbing in complex branched structures and on a variety of surfaces. Caterpillars therefore are excellent for examining the relationship between soft body deformation and substrate reaction forces during locomotion. In this study, we devised a method to measure the ground reaction forces (GRFs) at multiple contact points during crawling by the tobacco hornworm (Manduca sexta). Most abdominal prolegs bear similar body weight during their stance phase. Interestingly, forward reaction forces did not come from pushing off the substrate. Instead, most positive reaction forces came from anterior abdominal prolegs loaded in tension while posterior legs produced drag in most instances. The counteracting GRFs effectively stretch the animal axially during the second stage of a crawl cycle. These findings help in understanding how a terrestrial soft-bodied animal can interact with its substrate to control deformation without hydraulic actuation. The results also provide insights into the behavioral and mechanistic constraints leading to the evolution of diverse proleg arrangements in different species of caterpillar. [ABSTRACT FROM AUTHOR]

Unlike horizontal crawling, vertical crawling involves two counteracting forces: torque rotating the body around its center of mass and gravity resisting forward movement. The influence of these forces on kinematics has been examined in the soft-bodied larval stage of Manduca sexta. We found that crawling and climbing are accomplished using the same movements, with both segment timing and proleg lift indistinguishable in horizontal and vertical locomotion. Minor differences were detected in stride length and in the delay between crawls, which led to a lower crawling speed in the vertical orientation. Although these differences were statistically significant, they were much smaller than the variation in kinematic parameters between animals. The ability of Manduca to crawl and climb using the same movements is best explained by Manduca's relatively small size, slow speed and strong, controlled, passive grip made possible by its proleg/crochets. [ABSTRACT FROM AUTHOR]

In a wide variety of animals, stretch receptors provide proprioceptive feedback for motion control. However, for animals that lack a stiff skeleton, it is unclear what information is being detected and how this is incorporated into behavior. Because such animals can change their body shape from moment-to-moment, information about body configuration could be particularly important for coordination. This study uses larval stage Lepidoptera (Manduca sexta) to examine how the longitudinal stretch receptor organ (SRO) responds to behaviorally appropriate movements. We characterized the responses of the SRO to changes in strain using magnitudes and velocities matching those seen physiologically. We found that the SRO response characteristics are compatible with the regulation of stance and with the defensive response to noxious stimuli. However, we also found that movements during crawling produce SRO responses that are dominated by the interdependence of phasic, tonic and slowly adaptive components. Ablation of stretch receptors in the proleg-bearing, fourth abdominal segment did not have any observable effect on behaviors, which suggests that the SROs are not essential for coordinating overt movements. We discuss the implications of these findings in the context of specific behaviors, and explore how the SRO response might be utilized during animal behavior. [ABSTRACT FROM AUTHOR]

The development of truly biomimetic robots requires that soft materials be incorporated into the mechanical design and also used as an integral part of the motor control system. One approach to this challenge is to identify how soft animals control their movements and then apply the found principles in robotic applications. Here I show an example of how a combination of animal kinematics, neural patterning and constitutive modelling of tissues can be used to explore motor control in the caterpillar, Manduca sexta. Although still in the early stages, these findings are being used to design and fabricate a new type of robot that does not have a rigid skeleton and is structured entirely from soft or compliant materials. It is hoped that this new robotic platform will promote the development of actuators, sensors and electronics that are compatible with soft materials. [ABSTRACT FROM AUTHOR]

Caterpillars are soft-bodied terrestrial climbers that perform a wide variety of complex movements with several hundred muscles and a relatively small number of neurons. Control of movements is therefore expected to place unusual demands on the mechanical properties of the muscles. The muscles develop force slowly (1-6 s to peak) yet over a strain range extending from under 60% to more than 160% of resting length, with a length-tension relationship resembling that of supercontracting or cross-striated muscle. In passive and active sinusoidal strain cycling, muscles displayed viscoelastic qualities, with very low and stretch-velocity dependent resilience; there was a positive linear relationship between stretch velocity and the fraction of work dissipation attributable to passive muscle properties (20-80%). In linear stretches of unstimulated muscles at velocities bracketing those encountered in natural crawling, the rise in tension showed a distinct transition to a lower rate of increase, with transition tension dependent upon stretch velocity; peak force was exponentially related to stretch velocity. When stretching ceased, force decayed exponentially, with slower decay associated with lower stretch velocities; the decay time constant was exponentially related to stretch velocity. From the kinematics of caterpillars crawling horizontally we determined that the ventral interior lateral muscle (VIL) of the third abdominal segment (A3) is at or near resting length for most of the crawl cycle, with a fairly linear shortening by 25-30% and re-lengthening occupying about 45% of cycle duration. Synchronized kinematic and EMG recordings showed that during horizontal crawling A3 VIL is stimulated as the muscle shortens from about 95% to 75% of its resting length. We subjected in vitro VIL preparations to strain cycling and stimulus phase and duration similar to that of natural crawling. The resulting work loops were figure-eight shaped, with the muscle performing work during the shortest 45-65% of the strain cycle but dissipating work during the rest of the cycle. The muscle remained in the ascending limb of its length-tension relationship throughout the crawl cycle. Peak force occurred at the end of re-lengthening, nearly a full second after stimulation ceased, underscoring the importance of understanding passive muscle properties to explain caterpillar locomotion. Whether A3 VIL functions as an actuator at all during simulated natural strain cycling is highly sensitive to stimulus timing but far less so to stimulus duration. The muscle's elastomer-like properties appear to play a major role in its function. [ABSTRACT FROM AUTHOR]

Caterpillars are ecologically successful soft-bodied climbers. They are able to grip tightly to foliage using cuticular hooks at the tips of specialized abdominal limbs called prolegs. The neural control of proleg retraction has been examined in some detail but little is known about how prolegs extend and adduct. This is of particular interest because there are no extensor muscles or any obvious mechanisms for directing hydraulic flow into the proleg. In restrained tobacco hornworms (Manduca sexta), adduction can be evoked by stimulating mechanosensory hairs on the medial surface of the proleg. 3-D kinematics show that extension and adduetion occur simultaneously through an unfolding of membrane between the pseudo segments. Hemolymph pressure pulses are not necessary to extend the proleg; instead, the pressure at the base of the proleg decreases before adduetion and increases before retraction. It is proposed that these pressure changes are caused by muscles that stiffen and relax the body wall during cycles of retraction and adduction. Electromyographic recordings show that relaxation of the principal planta retractor muscle is essential for normal adduction. Extracellular nerve and muscle recordings in reduced preparations show that medial hair stimulation of one proleg can strongly and bilaterally excite motoneurons controlling the ventral internal lateral muscles of all the proleg-bearing segments. Ablation, nerve section and electromyographic experiments show that this muscle is not essential for adduction in restrained larvae but that it is coactive with the retractors and may be responsible for stiffening the body wall during proleg movements. [ABSTRACT FROM AUTHOR]

Abstract: The mechanical properties of soft tissues are important for the control of motion in many invertebrates. Pressurized cylindrical animals such as worms have circumferential reinforcement of the body wall; however, no experimental characterization of comparable anisotropy has been reported for climbing larvae such as caterpillars. Using uniaxial, real-time fluorescence extensometry on millimeter scale cuticle specimens we have quantified differences in the mechanical properties of cuticle to circumferentially and longitudinally applied forces. Based on these results and the composite matrix–fiber structure of cuticle, a pseudo-elastic transversely isotropic constitutive material model was constructed with circumferential reinforcement realized as a Horgan–Saccomandi strain energy function. This model was then used numerically to describe the anisotropic material properties of Manduca cuticle. The constitutive material model will be used in a detailed finite-element analysis to improve our understanding of the mechanics of caterpillar crawling. [Copyright &y& Elsevier]

Summary: Animals with an open coelom do not fully constrain internal tissues [], and changes in tissue or organ position during body movements cannot be readily discerned from outside of the body. This complicates modeling of soft-bodied locomotion, because it obscures potentially important changes in the center of mass as a result of internal tissue movements []. We used phase-contrast synchrotron X-ray imaging [] and transmission light microscopy to directly visualize internal soft-tissue movements in freely crawling caterpillars. Here we report a novel visceral-locomotory piston in crawling Manduca sexta larvae, in which the gut slides forward in advance of surrounding tissues. The initiation of gut sliding is synchronous with the start of the terminal prolegs'' swing phase, suggesting that the animal''s center of mass advances forward during the midabdominal prolegs'' stance phase and is therefore decoupled from visible translations of the body. Based on synchrotron X-ray data and transmission light microscopy results, we present evidence for a two-body mechanical system with a nonlinear elastic gut that changes size and translates between the anterior and posterior of the animal. The proposed two-body system—the container and the contained—is unlike any form of legged locomotion previously reported and represents a new feature in our emerging understanding of crawling. Video Abstract: Display Omitted [Copyright &y& Elsevier]