Barry A. Trimmer

Soft robotics: a bioinspired evolution in robotics

Animals exploit soft structures to move effectively in complex natural environments. These capabilities have inspired robotic engineers to incorporate soft technologies into their designs. The goal is to endow robots with new, bioinspired capabilities that permit adaptive, flexible interactions with unpredictable environments. Here, we review emerging soft-bodied robotic systems, and in particular recent developments inspired by soft-bodied animals. Incorporating soft technologies can potentially reduce the mechanical and algorithmic complexity involved in robot design. Incorporating soft technologies will also expedite the evolution of robots that can safely interact with humans and natural environments. Finally, soft robotics technology can be combined with tissue engineering to create hybrid systems for medical applications.

GoQBot: a caterpillar-inspired soft-bodied rolling robot

Rolling locomotion using an external force such as gravity has evolved many times. However, some caterpillars can curl into a wheel and generate their own rolling momentum as part of an escape repertoire. This change in body conformation occurs well within 100 ms and generates a linear velocity over 0.2 m s(-1), making it one of the fastest self-propelled wheeling behaviors in nature. Inspired by this behavior, we construct a soft-bodied robot to explore the dynamics and control issues of ballistic rolling. This robot, called GoQBot, closely mimics caterpillar rolling. Analyzing the whole body kinematics and 2D ground reaction forces at the robot ground anchor reveals about 1G of acceleration and more than 200 rpm of angular velocity. As a novel rolling robot, GoQBot demonstrates how morphing can produce new modes of locomotion. Furthermore, mechanical coupling of the actuators improves body coordination without sensory feedback. Such coupling is intrinsic to soft-bodied animals because there are no joints to isolate muscle-generated movements. Finally, GoQBot provides an estimate of the mechanical power for caterpillar rolling that is comparable to that of a locust jump. How caterpillar musculature produces such power in such a short time is yet to be discovered.

Current excitement from insect muscarinic receptors

Recent electrophysiological, pharmacological and molecular studies suggest that muscarinic ACh receptors (mAChRs) in insects are related to, but distinct from, their mammalian counterparts. Insect mAChRs perform two primary roles that are distinguished by their locations. Presynaptic mAChRs, present on sensory terminals, inhibit transmitter release, thereby reducing the effectiveness of specific afferent inputs. In contrast, postsynaptic mAChRs depolarize and increase the excitability of motoneurons and interneurons, thereby acting as dynamic-gain controls. This postsynaptic modulation is achieved in different ways in specific neurons but generally results from the activation of persistent inward and outward currents. At the level of neural processing, these distinct roles enable insect mAChRs to regulate the transfer of sensory information, and modulate the contributions of central neurons to central pattern generators and reflexes. Because these phenomena can be studied in identified neurons, a combination of physiological and molecular studies of mAChRs in insects should help to elucidate some of their behavioral roles. Furthermore, such studies could lead to the identification of general mechanisms of functional plasticity in neuronal networks.

Modulation of potassium channel function confers a hyperproliferative invasive phenotype on embryonic stem cells

Ion transporters, and the resulting voltage gradients and electric fields, have been implicated in embryonic development and regeneration. These biophysical signals are key physiological aspects of the microenvironment that epigenetically regulate stem and tumor cell behavior. Here, we identify a previously unrecognized function for KCNQ1, a potassium channel known to be involved in human Romano–Ward and Jervell–Lange–Nielsen syndromes when mutated. Misexpression of its modulatory wild-type β-subunit XKCNE1 in the Xenopus embryo resulted in a striking alteration of the behavior of one type of embryonic stem cell: the pigment cell lineage of the neural crest. Depolarization of embryonic cells by misexpression of KCNE1 non-cell-autonomously induced melanocytes to overproliferate, spread out, and become highly invasive of blood vessels, liver, gut, and neural tube, leading to a deeply hyperpigmented phenotype. This effect is mediated by the up-regulation of Sox10 and Slug genes, thus linking alterations in ion channel function to the control of migration, shape, and mitosis rates during embryonic morphogenesis. Taken together, these data identify a role for the KCNQ1 channel in regulating key cell behaviors and reveal the molecular identity of a biophysical switch, by means of which neoplastic-like properties can be conferred upon a specific embryonic stem cell subpopulation.

A constitutive model for muscle properties in a soft-bodied arthropod

In this paper, we examine the mechanical properties of muscles in a soft-bodied arthropod under both passive and stimulated conditions. In particular, we examine the ventral interior lateral muscle of the tobacco hornworm caterpillar, Manduca sexta, and show that its response is qualitatively similar to the behaviour of particle-reinforced rubber. Both materials are capable of large nonlinear elastic deformations, show a hysteretic behaviour and display stress softening during the first few cycles of repeated loading. The Manduca muscle can therefore be considered as different elastic materials during loading and unloading and is best described using the theory of pseudo-elasticity. We summarize the basic equations for transversely isotropic pseudo-elastic materials, first for general deformations and then for the appropriate uniaxial specialization. The constitutive relation proposed is in good agreement with the experimental data for both the passive and the stimulated conditions.

Kinematics of Soft-bodied, Legged Locomotion in Manduca sexta Larvae

Caterpillar crawling is distinct from that of worms and molluscs; it consists of a series of steps in different body segments that can be compared to walking and running in animals with stiff skeletons. Using a three-dimensional kinematic analysis of horizontal crawling in Manduca sexta, the tobacco hornworm, we found that the phase of vertical displacement in the posterior segments substantially led changes in horizontal velocity and the segments appeared to pivot around the attached claspers. Both of the motions occur during vertebrate walking. In contrast, vertical displacement and horizontal velocity in the anterior proleg-bearing segments were in phase, as expected for running gaits coupled by elastic storage. We propose that this kinematic similarity to running results from the muscular compression and release of elastic tissues. As evidence in support of this proposal, the compression and extension of each segment were similar to harmonic oscillations in a spring, although changes in velocity were 70° out of phase with displacement, suggesting that the spring was damped. Measurements of segment length within, and across, intersegmental boundaries show that some of these movements were caused by folding of the body wall between segments. These findings demonstrate that caterpillar crawling is not simply the forward progression of a peristaltic wave but has kinetic components that vary between segments. Although these movements can be compared to legged locomotion in animals with stiff skeletons, the underlying mechanisms of caterpillar propulsion, and in particular the contribution of elastic tissues, remain to be discovered.

The biomechanical and neural control of hydrostatic limb movements in Manduca sexta.

SUMMARY 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 adduction 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 adduction 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.

Flexible parylene-based microelectrode arrays for high resolution EMG recordings in freely moving small animals.

We present the development, fabrication and in vivo testing of a minimally invasive microelectrode array intended for high resolution multichannel recordings of electromyographic (EMG) signals. Parylene C was chosen as the structural substrate for its mechanical, electrical and physical properties. In particular, the device is extremely flexible. This provides a highly conformal coverage of the muscle surface and, at the same time, some degree of strain relief against the forces of micro-motion between the electrode and the surrounding tissues. By flexing and shaping itself to the muscles, the array is capable of maintaining a more stable electrical contact resulting in a significantly improved signal to noise ratio (SNR). To yield high signal selectivity, the design of the microelectrode array has been custom tailored to match the muscle anatomy of a particular animal system, the tobacco hornworm Manduca sexta. However, using the same fabrication protocol but different design parameters, the microdevice presented here can be easily implemented to study motor control and motor coordination in a vast range of small animals.

Nicotinic-acetylcholine receptors are functionally coupled to the nitric oxide/cGMP-pathway in insect neurons.

In addition to their ionotropic role, neuronal nicotinic acetylcholine receptors (nAChRs) can influence second messenger levels, transmitter release and gene transcription. In this study, we show that nAChRs in an insect CNS control cGMP levels by coupling to NO production. In conditions that inhibit spiking, nicotine induced cGMP synthesis. This increase in cGMP was blocked by nicotinic antagonists, and by inhibitors of both nitric oxide synthase and soluble guanylyl cyclase. The nicotinic‐evoked increase in cGMP was localized to specific NO‐sensitive neurons in the CNS, several of which are identified motoneurons. Because NO production requires Ca2+, we investigated the effect of nicotinic stimulation on [Ca2+]i in cultured neurons. We found that activation of nAChRs increased [Ca2+]i, which was blocked by nAChR antagonists. Nicotinic stimulation of neurons in the isolated CNS in low‐Na+, also evoked increases in [Ca2+]i independent of fast changes in voltage. In addition, approximately 10% of the nicotinic‐evoked [Ca2+]i increase in cultured neurons persisted when voltage‐gated Ca2+ channels were blocked by Ni2+. Under the same conditions, nicotinic stimulation of cGMP in the CNS was unaffected. These combined results suggest that nicotinic stimulation is coupled to NOS potentially by directly gating Ca2+.

Soft-cuticle biomechanics: a constitutive model of anisotropy for caterpillar integument.

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.