Till Bockemühl

Inter-leg coordination in the control of walking speed in Drosophila

SUMMARY Legged locomotion is the most common behavior of terrestrial animals and it is assumed to have become highly optimized during evolution. Quadrupeds, for instance, use distinct gaits that are optimal with regard to metabolic cost and have characteristic kinematic features and patterns of inter-leg coordination. In insects, the situation is not as clear. In general, insects are able to alter inter-leg coordination systematically with locomotion speed, producing a continuum of movement patterns. This notion, however, is based on the study of several insect species, which differ greatly in size and mass. Each of these species tends to walk at a rather narrow range of speeds. We have addressed these issues by examining four strains of Drosophila, which are similar in size and mass, but tend to walk at different speed ranges. Our data suggest that Drosophila controls its walking speed almost exclusively via step frequency. At high walking speeds, we invariably found tripod coordination patterns, the quality of which increased with speed as indicated by a simple measure of tripod coordination strength (TCS). At low speeds, we also observed tetrapod coordination and wave gait-like walking patterns. These findings not only suggest a systematic speed dependence of inter-leg movement patterns but also imply that inter-leg coordination is flexible. This was further supported by amputation experiments in which we examined walking behavior in animals after the removal of a hindleg. These animals show immediate adaptations in body posture, leg kinematics and inter-leg coordination, thereby maintaining their ability to walk.

Inter-joint coupling and joint angle synergies of human catching movements

A central question in motor control is how the central nervous system (CNS) deals with redundant degrees of freedom (DoFs) inherent in the musculoskeletal system. One way to simplify control of a redundant system is to combine several DoFs into synergies. In reaching movements of the human arm, redundancy occurs at the kinematic level because there is an unlimited number of arm postures for each position of the hand. Redundancy also occurs at the level of muscle forces because each arm posture can be maintained by a set of muscle activation patterns. Both postural and force-related motor synergies may contribute to simplify the control problem. The present study analyzes the kinematic complexity of natural, unrestrained human arm movements, and detects the amount of kinematic synergy in a vast variety of arm postures. We have measured inter-joint coupling of the human arm and shoulder girdle during fast, unrestrained, and untrained catching movements. Participants were asked to catch a ball launched towards them on 16 different trajectories. These had to be reached from two different initial positions. Movement of the right arm was recorded using optical motion capture and was transformed into 10 joint angle time courses, corresponding to 3 DoFs of the shoulder girdle and 7 of the arm. The resulting time series of the arm postures were analyzed by principal components analysis (PCA). We found that the first three principal components (PCs) always captured more than 97% of the variance. Furthermore, subspaces spanned by PC sets associated with different catching positions varied smoothly across the arms workspace. When we pooled complete sets of movements, three PCs, the theoretical minimum for reaching in 3D space, were sufficient to explain 80% of the datas variance. We assumed that the linearly correlated DoFs of each significant PC represent cardinal joint angle synergies, and showed that catching movements towards a multitude of targets in the arms workspace can be generated efficiently by linear combinations of three of such synergies. The contribution of each synergy changed during a single catching movement and often varied systematically with target location. We conclude that unrestrained, one-handed catching movements are dominated by strong kinematic couplings between the joints that reduce the kinematic complexity of the human arm and shoulder girdle to three non-redundant DoFs.

Speed-dependent interplay between local pattern-generating activity and sensory signals during walking in Drosophila

ABSTRACT In insects, the coordinated motor output required for walking is based on the interaction between local pattern-generating networks providing basic rhythmicity and leg sensory signals, which modulate this output on a cycle-to-cycle basis. How this interplay changes speed-dependently and thereby gives rise to the different coordination patterns observed at different speeds is not sufficiently understood. Here, we used amputation to reduce sensory signals in single legs and decouple them mechanically during walking in Drosophila. This allowed for the dissociation between locally generated motor output in the stump and coordinating influences from intact legs. Leg stumps were still rhythmically active during walking. Although the oscillatory frequency in intact legs was dependent on walking speed, stumps showed a high and relatively constant oscillation frequency at all walking speeds. At low walking speeds we found no strict cycle-to-cycle coupling between stumps and intact legs. In contrast, at high walking speeds stump oscillations were strongly coupled to the movement of intact legs on a one-to-one basis. Although during slow walking there was no preferred phase between stumps and intact legs, we nevertheless found a preferred time interval between touch-down or lift-off events in intact legs and levation or depression of stumps. Based on these findings, we hypothesize that, as in other insects, walking speed in Drosophila is predominantly controlled by indirect mechanisms and that direct modulation of basic pattern-generating circuits plays a subsidiary role. Furthermore, inter-leg coordination strength seems to be speed-dependent and greater coordination is evident at higher walking speeds. Summary: Leg amputation in fruit flies reveals that during walking inter-leg coordination strength increases with walking speed, thereby facilitating strict coordination during fast locomotion.

Intra- and intersegmental influences among central pattern generating networks in the walking system of the stick insect

To efficiently move around, animals need to coordinate their limbs. Proper, context-dependent coupling among the neural networks underlying leg movement is necessary for generating intersegmental coordination. In the slow-walking stick insect, local sensory information is very important for shaping coordination. However, central coupling mechanisms among segmental central pattern generators (CPGs) may also contribute to this. Here, we analyzed the interactions between contralateral networks that drive the depressor trochanteris muscle of the legs in both isolated and interconnected deafferented thoracic ganglia of the stick insect on application of pilocarpine, a muscarinic acetylcholine receptor agonist. Our results show that depressor CPG activity is only weakly coupled between all segments. Intrasegmental phase relationships differ between the three isolated ganglia, and they are modified and stabilized when ganglia are interconnected. However, the coordination patterns that emerge do not resemble those observed during walking. Our findings are in line with recent studies and highlight the influence of sensory input on coordination in slowly walking insects. Finally, as a direct interaction between depressor CPG networks and contralateral motoneurons could not be observed, we hypothesize that coupling is based on interactions at the level of CPG interneurons.NEW & NOTEWORTHY Maintaining functional interleg coordination is vitally important as animals locomote through changing environments. The relative importance of central mechanisms vs. sensory feedback in this process is not well understood. We analyzed coordination among the neural networks generating leg movements in stick insect preparations lacking phasic sensory feedback. Under these conditions, the networks governing different legs were only weakly coupled. In stick insect, central connections alone are thus insufficient to produce the leg coordination observed behaviorally.

Six-legged walking in insects: how CPGs, peripheral feedback, and descending signals generate coordinated and adaptive motor rhythms

Walking is a rhythmic locomotor behavior of legged animals, and its underlying mechanisms have been the subject of neurobiological research for more than 100 years. In this article, we review relevant historical aspects and contemporary studies in this field of research with a particular focus on the role of central pattern generating networks (CPGs) and their contribution to the generation of six-legged walking in insects. Aspects of importance are the generation of single-leg stepping, the generation of interleg coordination, and how descending signals influence walking. We first review how CPGs interact with sensory signals from the leg in the generation of leg stepping. Next, we summarize how these interactions are modified in the generation of motor flexibility for forward and backward walking, curve walking, and speed changes. We then review the present state of knowledge with regard to the role of CPGs in intersegmental coordination and how CPGs might be involved in mediating descending influences from the brain for the initiation, maintenance, modification, and cessation of the motor output for walking. Throughout, we aim to specifically address gaps in knowledge, and we describe potential future avenues and approaches, conceptual and methodological, with the latter emphasizing in particular options arising from the advent of neurogenetic approaches to this field of research and its combination with traditional approaches.

Body side-specific control of motor activity during turning in a walking animal

Animals and humans need to move deftly and flexibly to adapt to environmental demands. Despite a large body of work on the neural control of walking in invertebrates and vertebrates alike, the mechanisms underlying the motor flexibility that is needed to adjust the motor behavior remain largely unknown. Here, we investigated optomotor-induced turning and the neuronal mechanisms underlying the differences between the leg movements of the two body sides in the stick insect Carausius morosus. We present data to show that the generation of turning kinematics in an insect are the combined result of descending unilateral commands that change the leg motor output via task-specific modifications in the processing of local sensory feedback as well as modification of the activity of local central pattern generating networks in a body-side-specific way. To our knowledge, this is the first study to demonstrate the specificity of such modifications in a defined motor task. DOI: http://dx.doi.org/10.7554/eLife.13799.001

Direction-Specific Footpaths Can Be Predicted by the Motion of a Single Point on the Body of the Fruit Fly Drosophila Melanogaster

This work presents a probabilistic mathematical model for generating footpaths in an insect’s frame of reference, based on its body’s (i.e. thorax’s) motion in the ground frame of reference. This model uses digitized video data of fruit flies walking freely on a transparent surface to track the location of each foot and the motion of the body while in stance phase. We use this data to tune a rigid body kinematic model that predicts the motion of the feet, given the body’s motion. The result is a model that can be used to study other aspects of insect locomotion, or used to generate stepping motions for an insect-like robot.

Static stability predicts the continuum of interleg coordination patterns in Drosophila

ABSTRACT During walking, insects must coordinate the movements of their six legs for efficient locomotion. This interleg coordination is speed dependent: fast walking in insects is associated with tripod coordination patterns, whereas slow walking is associated with more variable, tetrapod-like patterns. To date, however, there has been no comprehensive explanation as to why these speed-dependent shifts in interleg coordination should occur in insects. Tripod coordination would be sufficient at low walking speeds. The fact that insects use a different interleg coordination pattern at lower speeds suggests that it is more optimal or advantageous at these speeds. Furthermore, previous studies focused on discrete tripod and tetrapod coordination patterns. Experimental data, however, suggest that changes observed in interleg coordination are part of a speed-dependent spectrum. Here, we explore these issues in relation to static stability as an important aspect for interleg coordination in Drosophila. We created a model that uses basic experimentally measured parameters in fruit flies to find the interleg phase relationships that maximize stability for a given walking speed. The model predicted a continuum of interleg coordination patterns spanning the complete range of walking speeds as well as an anteriorly directed swing phase progression. Furthermore, for low walking speeds, the model predicted tetrapod-like patterns to be most stable, whereas at high walking speeds, tripod coordination emerged as most optimal. Finally, we validated the basic assumption of a continuum of interleg coordination patterns in a large set of experimental data from walking fruit flies and compared these data with the model-based predictions. Summary: A simple stability-based modeling approach can explain why walking insects use different leg coordination patterns in a speed-dependent way.