Chris J. Dallmann

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.

The role of vibration in tactile speed perception

The relative motion between the surface of an object and our fingers produces patterns of skin deformation such as stretch, indentation, and vibrations. In this study, we hypothesized that motion-induced vibrations are combined with other tactile cues for the discrimination of tactile speed. Specifically, we hypothesized that vibrations provide a critical cue to tactile speed on surfaces lacking individually detectable features like dots or ridges. Thus masking vibrations unrelated to slip motion should impair the discriminability of tactile speed, and the effect should be surface-dependent. To test this hypothesis, we measured the precision of participants in discriminating the speed of moving surfaces having either a fine or a ridged texture, while adding masking vibratory noise in the working range of the fast-adapting mechanoreceptive afferents. Vibratory noise significantly reduced the precision of speed discrimination, and the effect was much stronger on the fine-textured than on the ridged surface. On both surfaces, masking vibrations at intermediate frequencies of 64 Hz (65-μm peak-to-peak amplitude) and 128 Hz (10 μm) had the strongest effect, followed by high-frequency vibrations of 256 Hz (1 μm) and low-frequency vibrations of 32 Hz (50 and 25 μm). These results are consistent with our hypothesis that slip-induced vibrations concur to the discrimination of tactile speed.

Mechanical processing via passive dynamic properties of the cockroach antenna can facilitate control during rapid running

The integration of information from dynamic sensory structures operating on a moving body is a challenge for locomoting animals and engineers seeking to design agile robots. As a tactile sensor is a physical linkage mediating mechanical interactions between body and environment, mechanical tuning of the sensor is critical for effective control. We determined the open-loop dynamics of a tactile sensor, specifically the antenna of the American cockroach, Periplaneta americana, an animal that escapes predators by using its antennae during rapid closed-loop tactilely mediated course control. Geometrical measurements and static bending experiments revealed an exponentially decreasing flexural stiffness (EI) from base to tip. Quasi-static experiments with a physical model support the hypothesis that a proximodistally decreasing EI can simplify control by increasing preview distance and allowing effective mapping to a putative control variable – body-to-wall distance – compared with an antenna with constant EI. We measured the free response at the tip of the antenna following step deflections and determined that the antenna rapidly damps large deflections: over 90% of the perturbation is rejected within the first cycle, corresponding to almost one stride period during high-speed running (~50 ms). An impulse-like perturbation near the tip revealed dynamics that were characteristic of an inelastic collision, keeping the antenna in contact with an object after impact. We contend that proximodistally decreasing stiffness, high damping and inelasticity simplify control during high-speed tactile tasks by increasing preview distance, providing a one-dimensional map between antennal bending and body-to-wall distance, and increasing the reliability of tactile information.

Motor flexibility in insects: Adaptive coordination of limbs in locomotion and near-range exploration

In recent years, research on insect motor behaviour―locomotion in particular―has provided a number of important new insights, many of which became possible because of methodological advances in motion capture of unrestrained moving insects. Behavioural analyses have not only backed-up neurophysiological analyses of the underlying mechanisms at work, they have also highlighted the complexity and variability of leg movements in naturalistic, unrestrained behaviour. Here, we argue that the variability of unrestrained motor behaviour should be considered a sign of behavioural flexibility. Assuming that variation of movement-related parameters is governed by neural mechanisms, behavioural analyses can complement neurophysiological investigations, for example by (i) dissociating distinct movement episodes based on functional and statistical grounds, (ii) quantifying when and how transitions between movement episodes occur, and (iii) dissociating temporal and spatial coordination. The present review emphasises the importance of considering the functional diversity of limb movements in insect behaviour. In particular, we highlight the fundamental difference between leg movements that generate interaction forces as opposed to those that do not. On that background, we discuss the spatially continuous modulation of swing movements and the quasi-rhythmic nature of stepping across insect orders. Based on examples of motor flexibility in stick insects, we illustrate the relevance of behaviour-based approaches for computational modelling of a rich and adaptive movement repertoire. Finally, we emphasise the intimate interplay of locomotion and near-range exploration. We propose that this interplay, through continuous integration of distributed, multimodal sensory feedback, is key to locomotor flexibility.

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.

Force Contribution of Single Leg Joints in a Walking Hexapod

We study leg joint torques of a large insect (Carausius morosus) to infer the functions of individual joints in closed kinematic chains during unrestrained walking. Leg joints were found to differentially contribute to multiple locomotor functions of a leg, such as body weight support and propulsion. We conclude that quantifying joint torques in freely behaving hexapods may provide a powerful tool in unraveling the feedback control strategies underlying motor flexibility.