A hierarchical model for external electrical control of an insect, accounting for inter-individual variation of muscle force properties.

Cyborg control of insect movement is promising for developing miniature, high-mobility, and efficient biohybrid robots. However, considering the inter-individual variation of the insect neuromuscular apparatus and its neural control is challenging. We propose a hierarchical model including inter-individual variation of muscle properties of three leg muscles involved in propulsion (retractor coxae), joint stiffness (pro- and retractor coxae), and stance-swing transition (protractor coxae and levator trochanteris) in the stick insect Carausius morosus. To estimate mechanical effects induced by external muscle stimulation, the model is based on the systematic evaluation of joint torques as functions of electrical stimulation parameters. A nearly linear relationship between the stimulus burst duration and generated torque was observed. This stimulus-torque characteristic holds for burst durations of up to 500ms, corresponding to the stance and swing phase durations of medium to fast walking stick insects. Hierarchical Bayesian modeling revealed that linearity of the stimulus-torque characteristic was invariant, with individually varying slopes. Individual prediction of joint torques provides significant benefits for precise cyborg control.

Hybrid insect-computer robots ­ an exciting fusion of biology and technology ­ herald a future of small, highly mobile and efficient devices. However, these robots require a way to control the movements of the insects, a task made complex due to the differences between different insects' nervous and muscle systems. To bridge this gap, Owaki, Dürr and Schmitz studied the relationship between electrical stimulation of three leg muscles in the legs of stick insects and the resultant torque. To do these experiments, the scientists kept the body of the stick insects fixed and electrically stimulated one out of three leg muscles to produce walking-like movements. The results of these electrical stimulations allowed Owaki, Dürr and Schmitz to propose a model that predicts the torque created in the insect's joints when different patterns of electrical stimulation are applied to a leg muscle. The researchers identified a near-linear relationship between the duration of the electrical stimulus and the resultant torque. Moreover, the slope of this linear relationship can be estimated for individual animals with a few measurements only. This finding refines the precision of the motor control required to build individually tuned biohybrid robots. Investigating the precise control of insect biohybrid robots, particularly using stick insects, can lead to advancements in biohybrid robotics and enrich our understanding of insect locomotion. Owaki, Dürr and Schmitz's insights could lead to the creation of adaptable and highly mobile devices with many applications, but key challenges need to be addressed. First, model testing must be implemented in free-walking insects, and the electrical stimuli must be refined to mimic natural neuromuscular signals more closely.

Locomotor resilience through load-dependent modulation of muscle co-contraction.

Terrestrial locomotor behavior in variable environments requires resilience to sudden changes in substrate properties. For example, walking animals can adjust to substantial changes in slope and corresponding changes in load distribution among legs. In insects, slope-dependent adjustments have mainly been examined under steady-state conditions, whereas the transition dynamics have been largely neglected. In a previous study, we showed that steady-state adjustments of stick insects to ±45 deg slopes involve substantial changes in joint torques and muscle activity with only minor changes in leg kinematics. Here, we took a close look at the time course of these adjustments as stick insects compensate for various kinds of disturbances to load distribution. In particular, we tested whether the transition from one steady state to another involves distinct transition steps or follows a graded process. To resolve this, we combined simultaneous recordings of whole-body kinematics and hindleg muscle activity to elucidate how freely walking Carausius morosus negotiated a step-change in substrate slope. Step-by-step adjustments revealed that muscle activity changed in a graded manner as a function of body pitch relative to gravity. We further show analogous transient adjustment of muscle activity in response to destabilizing lift-off events of neighboring legs and the disappearance of antagonist co-activation during crawling episodes. Given these three examples of load-dependent regulation of antagonist muscle co-contraction, we conclude that stick insects respond to both transient and sustained changes in load distribution by regulating joint stiffness rather than through distinct transition steps.

Evaluation of force feedback in walking using joint torques as "naturalistic" stimuli.

Control of adaptive walking requires the integration of sensory signals of muscle force and load. We have studied how mechanoreceptors (tibial campaniform sensilla) encode "naturalistic" stimuli derived from joint torques of stick insects walking on a horizontal substrate. Previous studies showed that forces applied to the legs using the mean torque profiles of a proximal joint were highly effective in eliciting motor activities. However, substantial variations in torque direction and magnitude occurred at the more distal femorotibial joint, which can generate braking or propulsive forces and provide lateral stability. To determine how these forces are encoded, we used torque waveforms of individual steps that had maximum values in stance in the directions of flexion or extension. Analysis of kinematic data showed that the torques in different directions tended to occur in different ranges of joint angles. Variations within stance were not accompanied by comparable changes in joint angle but often reflected vertical ground reaction forces and leg support of body load. Application of torque waveforms elicited sensory discharges with variations in firing frequency similar to those seen in freely walking insects. All sensilla directionally encoded the dynamics of force increases and showed hysteresis to transient force decreases. Smaller receptors exhibited more tonic firing. Our findings suggest that dynamic sensitivity in force feedback can modulate ongoing muscle activities to stabilize distal joints when large forces are generated at proximal joints. Furthermore, use of "naturalistic" stimuli can reproduce characteristics seen in freely moving animals that are absent in conventional restrained preparations.NEW & NOTEWORTHY Sensory encoding of forces during walking by campaniform sensilla was characterized in stick insects using waveforms of joint torques calculated by inverse dynamics as mechanical stimuli. Tests using the mean joint torque and torques of individual steps showed the system is highly sensitive to force dynamics (dF/dt). Use of "naturalistic" stimuli can reproduce characteristics of sensory discharges seen in freely walking insects, such as load transfer among legs.

Integrative Biomimetics of Autonomous Hexapedal Locomotion.

Despite substantial advances in many different fields of neurorobotics in general, and biomimetic robots in particular, a key challenge is the integration of concepts: to collate and combine research on disparate and conceptually disjunct research areas in the neurosciences and engineering sciences. We claim that the development of suitable robotic integration platforms is of particular relevance to make such integration of concepts work in practice. Here, we provide an example for a hexapod robotic integration platform for autonomous locomotion. In a sequence of six focus sections dealing with aspects of intelligent, embodied motor control in insects and multipedal robots-ranging from compliant actuation, distributed proprioception and control of multiple legs, the formation of internal representations to the use of an internal body model-we introduce the walking robot HECTOR as a research platform for integrative biomimetics of hexapedal locomotion. Owing to its 18 highly sensorized, compliant actuators, light-weight exoskeleton, distributed and expandable hardware architecture, and an appropriate dynamic simulation framework, HECTOR offers many opportunities to integrate research effort across biomimetics research on actuation, sensory-motor feedback, inter-leg coordination, and cognitive abilities such as motion planning and learning of its own body size.

Motor control of an insect leg during level and incline walking.

During walking, the leg motor system must continually adjust to changes in mechanical conditions, such as the inclination of the ground. To understand the underlying control, it is important to know how changes in leg muscle activity relate to leg kinematics (movements) and leg dynamics (forces, torques). Here, we studied these parameters in hindlegs of stick insects (Carausius morosus) during level and uphill/downhill (±45 deg) walking, using a combination of electromyography, 3D motion capture and ground reaction force measurements. We find that some kinematic parameters including leg joint angles and body height vary across walking conditions. However, kinematics vary little compared with dynamics: horizontal leg forces and torques at the thorax-coxa joint (leg protraction/retraction) and femur-tibia joint (leg flexion/extension) tend to be stronger during uphill walking and are reversed in sign during downhill walking. At the thorax-coxa joint, the different mechanical demands are met by adjustments in the timing and magnitude of antagonistic muscle activity. Adjustments occur primarily in the first half of stance after the touch-down of the leg. When insects transition from level to incline walking, the characteristic adjustments in muscle activity occur with the first step of the leg on the incline, but not in anticipation. Together, these findings indicate that stick insects adjust leg muscle activity on a step-by-step basis so as to maintain a similar kinematic pattern under different mechanical demands. The underlying control might rely primarily on feedback from leg proprioceptors signaling leg position and movement.

Force dynamics and synergist muscle activation in stick insects: the effects of using joint torques as mechanical stimuli.

Many sensory systems are tuned to specific parameters of behaviors and have effects that are task-specific. We have studied how force feedback contributes to activation of synergist muscles in serially homologous legs of stick insects. Forces were applied using conventional half-sine or ramp and hold functions. We also utilized waveforms of joint torques calculated from experiments in freely walking animals. In all legs, forces applied to either the tarsus (foot) or proximal leg segment (trochanter) activated synergist muscles that generate substrate grip and support, but coupling of the depressor muscle to tarsal forces was weak in the front legs. Activation of trochanteral receptors using ramp and hold functions generated positive feedback to the depressor muscle in all legs when animals were induced to seek substrate grip. However, discharges of the synergist flexor muscle showed adaptation at moderate force levels. In contrast, application of forces using torque waveforms, which do not have a static hold phase, produced sustained discharges in muscle synergies with little adaptation. Firing frequencies reflected the magnitude of ground reaction forces, were graded to changes in force amplitude, and could also be modulated by transient force perturbations added to the waveforms. Comparison of synergist activation by torques and ramp and hold functions revealed a strong influence of force dynamics (dF/d t). These studies support the idea that force receptors can act to tune muscle synergies synchronously to the range of force magnitudes and dynamics that occur in each leg according to their specific use in behavior. NEW & NOTEWORTHY The effects of force receptors (campaniform sensilla) on leg muscles and synergies were characterized in stick insects using both ramp and hold functions and waveforms of joint torques calculated by inverse dynamics. Motor responses were sustained and showed reduced adaptation to the more "natural" and nonlinear torque stimuli. Calculation of the first derivative (dF/d t) of the torque waveforms demonstrated that this difference was correlated with the dynamic sensitivities of the system.

A load-based mechanism for inter-leg coordination in insects.

Animals rely on an adaptive coordination of legs during walking. However, which specific mechanisms underlie coordination during natural locomotion remains largely unknown. One hypothesis is that legs can be coordinated mechanically based on a transfer of body load from one leg to another. To test this hypothesis, we simultaneously recorded leg kinematics, ground reaction forces and muscle activity in freely walking stick insects (Carausius morosus). Based on torque calculations, we show that load sensors (campaniform sensilla) at the proximal leg joints are well suited to encode the unloading of the leg in individual steps. The unloading coincides with a switch from stance to swing muscle activity, consistent with a load reflex promoting the stance-to-swing transition. Moreover, a mechanical simulation reveals that the unloading can be ascribed to the loading of a specific neighbouring leg, making it exploitable for inter-leg coordination. We propose that mechanically mediated load-based coordination is used across insects analogously to mammals.

Effects of force detecting sense organs on muscle synergies are correlated with their response properties.

Sense organs that monitor forces in legs can contribute to activation of muscles as synergist groups. Previous studies in cockroaches and stick insects showed that campaniform sensilla, receptors that encode forces via exoskeletal strains, enhance muscle synergies in substrate grip. However synergist activation was mediated by different groups of receptors in cockroaches (trochanteral sensilla) and stick insects (femoral sensilla). The factors underlying the differential effects are unclear as the responses of femoral campaniform sensilla have not previously been characterized. The present study characterized the structure and response properties (via extracellular recording) of the femoral sensilla in both insects. The cockroach trochantero-femoral (TrF) joint is mobile and the joint membrane acts as an elastic antagonist to the reductor muscle. Cockroach femoral campaniform sensilla show weak discharges to forces in the coxo-trochanteral (CTr) joint plane (in which forces are generated by coxal muscles) but instead encode forces directed posteriorly (TrF joint plane). In stick insects, the TrF joint is fused and femoral campaniform sensilla discharge both to forces directed posteriorly and forces in the CTr joint plane. These findings support the idea that receptors that enhance synergies encode forces in the plane of action of leg muscles used in support and propulsion.

Joint torques in a freely walking insect reveal distinct functions of leg joints in propulsion and posture control.

Determining the mechanical output of limb joints is critical for understanding the control of complex motor behaviours such as walking. In the case of insect walking, the neural infrastructure for single-joint control is well described. However, a detailed description of the motor output in form of time-varying joint torques is lacking. Here, we determine joint torques in the stick insect to identify leg joint function in the control of body height and propulsion. Torques were determined by measuring whole-body kinematics and ground reaction forces in freely walking animals. We demonstrate that despite strong differences in morphology and posture, stick insects show a functional division of joints similar to other insect model systems. Propulsion was generated by strong depression torques about the coxa-trochanter joint, not by retraction or flexion/extension torques. Torques about the respective thorax-coxa and femur-tibia joints were often directed opposite to fore-aft forces and joint movements. This suggests a posture-dependent mechanism that counteracts collapse of the leg under body load and directs the resultant force vector such that strong depression torques can control both body height and propulsion. Our findings parallel propulsive mechanisms described in other walking, jumping and flying insects, and challenge current control models of insect walking.

Force feedback reinforces muscle synergies in insect legs.

The nervous system solves complex biomechanical problems by activating muscles in modular, synergist groups. We have studied how force feedback in substrate grip is integrated with effects of sense organs that monitor support and propulsion in insects. Campaniform sensilla are mechanoreceptors that encode forces as cuticular strains. We tested the hypothesis that integration of force feedback from receptors of different leg segments during grip occurs through activation of specific muscle synergies. We characterized the effects of campaniform sensilla of the feet (tarsi) and proximal segments (trochanter and femur) on activities of leg muscles in stick insects and cockroaches. In both species, mechanical stimulation of tarsal sensilla activated the leg muscle that generates substrate grip (retractor unguis), as well as proximal leg muscles that produce inward pull (tibial flexor) and support/propulsion (trochanteral depressor). Stimulation of campaniform sensilla on proximal leg segments activated the same synergistic group of muscles. In stick insects, the effects of proximal receptors on distal leg muscles changed and were greatly enhanced when animals made active searching movements. In insects, the task-specific reinforcement of muscle synergies can ensure that substrate adhesion is rapidly established after substrate contact to provide a stable point for force generation.

Task-dependent modification of leg motor neuron synaptic input underlying changes in walking direction and walking speed.

Animals modify their behavior constantly to perform adequately in their environment. In terrestrial locomotion many forms of adaptation exist. Two tasks are changes of walking direction and walking speed. We investigated these two changes in motor output in the stick insect Cuniculina impigra to see how they are brought about at the level of leg motor neurons. We used a semi-intact preparation in which we can record intracellularly from leg motor neurons during walking. In this single-leg preparation the middle leg of the animal steps in a vertical plane on a treadwheel. Stimulation of either abdomen or head reliably elicits fictive forward or backward motor activity, respectively, in the fixed and otherwise deafferented thorax-coxa joint. With a change of walking direction only thorax-coxa-joint motor neurons protractor and retractor changed their activity. The protractor switched from swing activity during forward to stance activity during backward walking, and the retractor from stance to swing. This phase switch was due to corresponding change of phasic synaptic inputs from inhibitory to excitatory and vice versa at specific phases of the step cycle. In addition to phasic synaptic input a tonic depolarization of the motor neurons was present. Analysis of changes in stepping velocity during stance showed only a significant correlation to flexor motor neuron activity, but not to that of retractor and depressor motor neurons during forward walking. These results show that different tasks in the stick insect walking system are generated by altering synaptic inputs to specific leg joint motor neurons only.

WITHDRAWN: Positive force feedback in development of substrate grip in the stick insect tarsus.

The Publisher regrets that this article is an accidental duplication of an article that has already been published, http://dx.doi.org/10.1016/j.asd.2014.06.002. The duplicate article has therefore been withdrawn.

Positive force feedback in development of substrate grip in the stick insect tarsus.

The mechanics of substrate adhesion has recently been intensively studied in insects but less is known about the sensorimotor control of substrate engagement. We characterized the responses and motor effects of tarsal campaniform sensilla in stick insects to understand how sensory signals of force could contribute to substrate grip. The tarsi consist of a chain of segments linked by highly flexible articulations. Morphological studies showed that one to four campaniform sensilla are located on the distal end of each segment. Activities of the receptors were recorded neurographically and sensilla were identified by stimulation and ablation of their cuticular caps. Responses were characterized to bending forces and axial loads, muscle contractions and to forces applied to the retractor apodeme (tendon). The tarsal sensilla effectively encoded both the rate and amplitude of loads and muscle forces, but only when movement was resisted. Mechanical stimulation of the receptors produced activation of motor neurons in the retractor unguis and tibial flexor muscles. These findings indicate that campaniform sensilla can provide information about the effectiveness of the leg muscles in generating substrate adherence. They can also produce positive force feedback that could contribute to the development of substrate grip and stabilization of the tarsal chain.

Directional specificity and encoding of muscle forces and loads by stick insect tibial campaniform sensilla, including receptors with round cuticular caps.

In many systems, loads are detected as the resistance to muscle contractions. We studied responses to loads and muscle forces in stick insect tibial campaniform sensilla, including a subgroup of receptors (Group 6B) with unusual round cuticular caps in oval-shaped collars. Loads were applied in different directions and muscle contractions were emulated by applying forces to the tibial flexor muscle tendon (apodeme). All sensilla 1) were maximally sensitive to loads applied in the plane of joint movement and 2) encoded muscle forces but did not discharge to unresisted movements. Identification of 6B sensilla by stimulation of cuticular caps demonstrated that receptor responses were correlated with their morphology. Sensilla with small cuticular collars produced small extracellular potentials, had low thresholds and strong tonic sensitivities that saturated at moderate levels. These receptors could effectively signal sustained loads. The largest spikes, derived from sensilla with large cuticular collars, had strong dynamic sensitivities and signaled a wide range of muscle forces and loads. Tibial sensilla are apparently tuned to produce no responses to inertial forces, as occur in the swing phase of walking. This conclusion is supported by tests in which animals 'stepped' on a compliant surface and sensory discharges only occurred in stance.

A hexapod walker using a heterarchical architecture for action selection.

Moving in a cluttered environment with a six-legged walking machine that has additional body actuators, therefore controlling 22 DoFs, is not a trivial task. Already simple forward walking on a flat plane requires the system to select between different internal states. The orchestration of these states depends on walking velocity and on external disturbances. Such disturbances occur continuously, for example due to irregular up-and-down movements of the body or slipping of the legs, even on flat surfaces, in particular when negotiating tight curves. The number of possible states is further increased when the system is allowed to walk backward or when front legs are used as grippers and cannot contribute to walking. Further states are necessary for expansion that allow for navigation. Here we demonstrate a solution for the selection and sequencing of different (attractor) states required to control different behaviors as are forward walking at different speeds, backward walking, as well as negotiation of tight curves. This selection is made by a recurrent neural network (RNN) of motivation units, controlling a bank of decentralized memory elements in combination with the feedback through the environment. The underlying heterarchical architecture of the network allows to select various combinations of these elements. This modular approach representing an example of neural reuse of a limited number of procedures allows for adaptation to different internal and external conditions. A way is sketched as to how this approach may be expanded to form a cognitive system being able to plan ahead. This architecture is characterized by different types of modules being arranged in layers and columns, but the complete network can also be considered as a holistic system showing emergent properties which cannot be attributed to a specific module.

Walknet, a bio-inspired controller for hexapod walking.

Walknet comprises an artificial neural network that allows for the simulation of a considerable amount of behavioral data obtained from walking and standing stick insects. It has been tested by kinematic and dynamic simulations as well as on a number of six-legged robots. Over the years, various different expansions of this network have been provided leading to different versions of Walknet. This review summarizes the most important biological findings described by Walknet and how they can be simulated. Walknet shows how a number of properties observed in insects may emerge from a decentralized architecture. Examples are the continuum of so-called "gaits," coordination of up to 18 leg joints during stance when walking forward or backward over uneven surfaces and negotiation of curves, dealing with leg loss, as well as being able following motion trajectories without explicit precalculation. The different Walknet versions are compared to other approaches describing insect-inspired hexapod walking. Finally, we briefly address the ability of this decentralized reactive controller to form the basis for the simulation of higher-level cognitive faculties exceeding the capabilities of insects.

Force encoding in stick insect legs delineates a reference frame for motor control.

The regulation of forces is integral to motor control. However, it is unclear how information from sense organs that detect forces at individual muscles or joints is incorporated into a frame of reference for motor control. Campaniform sensilla are receptors that monitor forces by cuticular strains. We studied how loads and muscle forces are encoded by trochanteral campaniform sensilla in stick insects. Forces were applied to the middle leg to emulate loading and/or muscle contractions. Selective sensory ablations limited activities recorded in the main leg nerve to specific receptor groups. The trochanteral campaniform sensilla consist of four discrete groups. We found that the dorsal groups (Groups 3 and 4) encoded force increases and decreases in the plane of movement of the coxo-trochanteral joint. Group 3 receptors discharged to increases in dorsal loading and decreases in ventral load. Group 4 showed the reverse directional sensitivities. Vigorous, directional responses also occurred to contractions of the trochanteral depressor muscle and to forces applied at the muscle insertion. All sensory discharges encoded the amplitude and rate of loading or muscle force. Stimulation of the receptors produced reflex effects in the depressor motoneurons that could reverse in sign during active movements. These data, in conjunction with findings of previous studies, support a model in which the trochanteral receptors function as an array that can detect forces in all directions relative to the intrinsic plane of leg movement. The array could provide requisite information about forces and simplify the control and adaptation of posture and walking.

Encoding of force increases and decreases by tibial campaniform sensilla in the stick insect, Carausius morosus.

Detection of force increases and decreases is important in motor control. Experiments were performed to characterize the structure and responses of tibial campaniform sensilla, receptors that encode forces through cuticular strains, in the middle leg of the stick insect (Carausius morosus). The sensilla consist of distinct subgroups. Group 6A sensilla are located 0.3 mm distal to the femoro-tibial joint and have oval shaped cuticular caps. Group 6B receptors are 1 mm distal to the joint and have round caps. All sensilla show directional, phasico-tonic responses to forces applied to the tibia in the plane of joint movement. Group 6B sensilla respond to force increases in the direction of joint extension while Group 6A receptors discharge when those forces decrease. Forces applied in the direction of joint flexion produce the reverse pattern of sensory discharge. All receptors accurately encode the rate of change of force increments and decrements. Contractions of tibial muscles also produce selective, directional sensory discharges. The subgroups differ in their reflex effects: Group 6B receptors excite and Group 6A sensilla inhibit tibial extensor and trochanteral depressor motoneurons. The tibial campaniform sensilla can, therefore, encode force increases or decreases and aid in adapting motor outputs to changes in load.

Tight turns in stick insects.

We investigated insects Carausius morosus walking whilst hanging upside down along a narrow 3 mm horizontal beam. At the end of the beam, the animal takes a 180 degrees turn. This is a difficult situation because substrate area is small and moves relative to the body during the turn. We investigated how leg movements are organised during this turn. A non-contact of either front leg appears to indicate the end of the beam. However, a turn can only begin if the hind legs stand in an appropriate position relative to each other; the outer hind leg must not be placed posterior to the inner hind leg. When starting the turn, both front legs are lifted and usually held in a relatively stable position and then the inner middle leg performs a swing-and-search movement: The leg begins a swing, which is continued by a searching movement to the side and to the rear, and eventually grasps the beam. At the same time the body is turned usually being supported by the outer middle leg and both hind legs. Then front legs followed by the outer middle leg reach the beam. A scheme describing the turns based on a few simple behavioural elements is proposed.

Winching up heavy loads with a compliant arm: a new local joint controller.

A closed kinematic chain, like an arm that operates a crank, has a constrained movement space. A meaningful movement of the chain's endpoint is only possible along the free movement directions which are given implicitly by the contour of the object that confines the movement of the chain. Many technical solutions for such a movement task, in particular those used in robotics, use central controllers and force-torque sensors in the arm's wrist or a leg's ankle to construct a coordinate system (task frame formalism) at the local point of contact the axes of which coincide with the free and constrained movement directions. Motivated by examples from biology, we introduce a new control system that solves a constrained movement task. The control system is inspired by the control architecture that is found in stick insects like Carausius morosus. It consists of decentral joint controllers that work on elastic joints (compliant manipulator). The decentral controllers are based on local positive velocity feedback (LPVF). It has been shown earlier that LPVF enables contour following of a limb in a compliant motion task without a central controller. In this paper we extend LPVF in such a way that it is even able to follow a contour if a considerable counter force drags the limb away along the contour in a direction opposite to the desired. The controller extension is based on the measurement of the local mechanical power generated in the elastic joint and is called power-controlled relaxation LPVF. The new control approach has the following advantages. First, it still uses local joint controllers without knowledge of the kinematics. Second, it does not need a force or torque measurement at the end of the limb. In this paper we test power-controlled relaxation LPVF on a crank turning task in which a weight has to be winched up by a two-joint compliant manipulator.