The control of walking movements in the leg of the rock lobster

1. Experiments with rock lobsters walking on a treadmill were undertaken to obtain information upon the system controlling the movement of the legs. Results show that the position of the leg is an important parameter affecting the cyclic movement of the walking leg. Stepping can be interrupted when the geometrical conditions for terminating either a return stroke or a power stroke are not fullfilled. 2. The mean value of anterior and posterior extreme positions (AEP and PEP respectively) of the walking legs do not depend on the walking speed (Fig. 1). 3. When one leg is isolated from the other walking legs by placing it on a platform the AEPs and PEPs of the other legs show a broader distribution compared to controls (Figs. 2 and 3). 4. Force measurements (Fig. 4) are in agreement with the hypothesis that the movement of the leg is controlled by a position servomechanism. 5. When one leg stands on a stationary force transducer this leg develops forces which oscillate with the step rhythm of the other legs (Fig. 5). 6. A posteriorly directed influence is found, by which the return stroke of a leg can be started when the anterior leg performs a backward directed movement. 7. Results are compared with those obtained from stick insects. The systems controlling the movement of the individual leg are similar in both, lobster and stick insect but the influences between the legs seem to be considerably different.     

The contralateral coordination of walking legs in the crayfish Astacus leptodactylus

The coupling mechanisms which coordinate the movement of ipsilateral walking legs in the crayfish have been described in earlier investigations. Concerning the coupling between contralateral legs it was only known that these influences are weaker than those acting between ipsilateral legs. The nature of these coupling mechanisms between contralateral legs of the crayfish are investigated here by running left and right legs on separate walking belts at different speeds. The results show that coordination is performed by a phase-dependent shift of the anterior extreme position of the influenced leg. This backward shift leads to a shortening of both the return stroke and the following power stroke. As the coupling influence is only weak, several steps might be necessary to retain normal coordination after a disturbance. This corresponds to v. Holst's relative coordination. The influences act in both directions, from left to right and vice versa. However, one side may be more or less dominant. A gradient was found in the way that anterior leg pairs show less strong coordination than posterior legs. In some cases the coupling between diagonally neighbouring legs was found to be stronger than between contralateral legs of the same segment. The interpretation of this result is still open.     

Comparison of forces developed by the leg of the rock lobster when walking free or on a treadmill

Summary In the free walking rock lobster the forces developed by legs 4 and 5 were investigated during the power stroke. Two orthogonal force components lying in the horizontal plane were measured. Based on these results the diffent tasks of the two legs during walking are discussed. The forces developed by leg 4 were compared when the animal walked freely and on a treadmill. In these two situations the results differ qualitatively as in driven walking the forces are nearly identical in a long series of consecutive steps whereas in free walking the forces can vary greatly from step to step. However, similar mean values of force were measured with those on the treadmill being somewhat higher. This shows that, although the treadmill is driven by a motor, the animal does perform active walking movements. In the treadmill situation the forces increase as the speed of treadmill motor is decreased.Supported by DAAD and DFG (Cr 58) for H. Cruse and by ATP (80 119.112) INSERM for F. Clarac     

Coordination between the legs and tail during digging and swimming in sand crabs

Rhythmic leg movements and tailflipping are mutually exclusive behaviours in most decapod crustaceans, but sand crabs (Anomura: Hippoidea) combine leg movements with simultaneous tailflipping or uropod beating for both digging and swimming. We examined the coordination between the legs and tail (abdomen and tailfan) of Blepharipoda occidentalis, Lepidopa californica (Albuneidae), and Emerita analoga (Hippidae). When either albuneid swims, the tail cycles at a higher frequency than the legs, and the two rhythms are not coupled. When albuneids begin digging, the tail's frequency drops to that of the legs, and its rhythm becomes phase coupled to the legs. In E. analoga the legs seldom move during swimming by uropod beating. During digging the frequency of the uropods and fourth legs starts at about double that of the second and third legs, but drops to that of the second and third legs as digging progresses. The fourth legs in E. analoga are coupled with the uropods; their outward movement (= power stroke) is concurrent with the uropod return stroke. The familial differences in leg coordination and in the coordination of the legs and tail account for the smooth descent of E. analoga beneath sand compared to the stepwise descent of the albuneids. Accepted: 23 August 1996     

A modular artificial neural net for controlling a six-legged walking system

 A system that controls the leg movement of an animal or a robot walking over irregular ground has to ensure stable support for the body and at the same time propel it forward. To do so, it has to react adaptively to unpredictable features of the environment. As part of our study of the underlying mechanisms, we present here a model for the control of the leg movement of a 6-legged walking system. The model is based on biological data obtained from the stick insect. It represents a combined treatment of realistic kinematics and biologically motivated, adaptive gait generation. The model extends a previous algorithmic model by substituting simple networks of artificial neurons for the algorithms previously used to control leg state and interleg coordination. Each system controlling an individual leg consists of three subnets. A hierarchically superior net contains two sensory and two ‘premotor’ units; it rhythmically suppresses the output of one or the other of the two subordinate nets. These are continuously active. They might be called the ‘swing module’ and the ‘stance module’ because they are responsible for controlling the swing (return stroke) and the stance (power stroke) movements, respectively. The swing module consists of three motor units and seven sensory units. It can produce appropriate return stroke movements for a broad range of initial and final positions, can cope with mechanical disturbances of the leg movement, and is able to react to an obstacle which hinders the normal performance of the swing movement. The complete model is able to walk at different speeds over irregular surfaces. The control system rapidly reestablishes a stable gait when the movement of the legs is disturbed. Received: 13 July 1994/Accepted in revised form: 15 November 1994     

Ants swimming in pitcher plants: kinematics of aquatic and terrestrial locomotion in Camponotus schmitzi

Camponotus schmitzi ants live in symbiosis with the Bornean pitcher plant Nepenthes bicalcarata. Unique among ants, the workers regularly dive and swim in the pitcher's digestive fluid to forage for food. High-speed motion analysis revealed that C.?schmitzi ants swim at the surface with all legs submerged, with an alternating tripod pattern. Compared to running, swimming involves lower stepping frequencies and larger phase delays within the legs of each tripod. Swimming ants move front and middle legs faster and keep them more extended during the power stroke than during the return stroke. Thrust estimates calculated from three-dimensional leg kinematics using a blade-element approach confirmed that forward propulsion is mainly achieved by the front and middle legs. The hind legs move much less, suggesting that they mainly serve for steering. Experiments with tethered C.?schmitzi ants showed that characteristic swimming movements can be triggered by submersion in water. This reaction was absent in another Camponotus species investigated. Our study demonstrates how insects can use the same locomotory system and similar gait patterns for moving on land and in water. We discuss insect adaptations for aquatic/amphibious lifestyles and the special adaptations of C.?schmitzi to living on an insect-trapping pitcher plant.     

Coordination of legs during straight walking and turning in Drosophila melanogaster

Leg coordination of Drosophila melanogaster was studied using frame-by-frame film analysis. 1. For fastest walking alternating tripod coordination is observed which slightly deviates towards tetrapody as a function of step period. During acceleration or deceleration legs may transiently recover in diagonal pairs. 2. Mean step length increases with step frequency. 3. Mean recovery stroke duration increases with step period and plateaus beyond a period of about 110 ms. Middle legs recover significantly faster than others. 4. Ipsilateral footprints are transversally separated. 5. Walking is usually initiated in tripod coordination (frequently in combination with a turn), otherwise in an accelerating sequence which rapidly shifts towards tripod pattern. Flies can stop abruptly or decelerate over about one metachronal wave. 6. Short interruptions in walking are observed. Legs interrupted during swing phase stay lifted and finish recovery thereafter. 7. Slight changes in walking direction are obtained by altering step lengths only. Tight turns are composed of two or three phases with backward, zero and forward translatory components. In fast turning tripod coordination is maintained. Otherwise body sides can decouple widely. In all turns numbers of contralateral metachronal waves were equal. Results are compared to those for other walking insects and their relevance in screens for locomotor mutants is discussed.     

Basic processes of locomotor coordination in the rock lobster

Rock lobsters are able to perform long and stereotyped stepping sequences above a motor driven treadmill. Forward walking samples are estimated by mean of statistical methods to draw out the basic rules involved in the locomotor behaviour (Fig. 1).

- The spatial and temporal parameters defined in a single propulsive leg are either invariable in respect to the imposed speed, as the mean step length (L), the return stroke duration (Tr) and the pause times (T's, T'r), or speed dependent as the power stroke duration (Ts) and the whole period (Figs. 2 and 3).

- The interleg phase coupling is strong and stable in the ipsilateral rear pairs (4–5), these legs acting most of the time in absolute coordination (1:1) or in harmonic ratio (2:1). In the contralateral pairs (R4-L4, R5-L5) the legs roughly operate in antiphase, but the relationship appears much weaker and variable, with frequent episodes of relative coordination (Fig. 4).

- The time intervals between the ground contact of any leg and the swing initiation in the nearest ones appear somewhat constant and could be closely related to the mechanism of stepping synchronization. The “5 on - 4 off” delay, very stable and always positive, suggests that the rear legs could exert a predominant influence upon the rhythmical movements of the next anterior ipsilateral appendages (Fig. 5).

- To test the contralateral relationships, the treadmill belts can be decoupled in order to impose different walking speeds on each side. Such a conflicting stimulus reveals that:

1. The relative hierarchy always observed between the ipsilateral legs can be artificially created between the two sides (Fig. 6).
2. The driving influence of a given leg is closely linked to the intensity of EMG's discharges in its power stroke muscles.
3. The contralateral appendages are able to walk in absolute coordination despite a large speed difference between the two sides (up to 4 cm/s). Under such a constraint, the walking legs alter its invariable parameters (L and Tr) to reach a common step period and steadily maintain the alternating pattern (Figs. 6 and 7).

     

Motor output to the protractor and retractor coxae muscles in stick insects walking on a treadwheel

ABSTRACT. The motor output to the protractor and retractor mucles moving the coxa of the middle leg of Carausius morosus was recorded from the thoracic nerves during walking on a treadwheel. The leg movements on the wheel were generally similar to those found in free-walking animals, but tripod coordination was relatively independent of period, and the coordination of the adult animal on the wheel was most closely related to that found in free-walking first instars. The activity of a common inhibitor and four excitatory axons of the retractor and an excitatory axon of the protractor were followed for 850 steps (in six animals) to give a summary of the behaviour of the different units. The motor activity is less stereotyped than that previously reported for insects. There was strong reciprocity between the antagonists, but this was not directly correlated with the forward and backward movements of the legs. The first part of the stance phase of the leg was accompanied by a strong burst in the protractor nerve and relatively little retractor activity. This was followed by the main retractor burst which occupied the last 60% of the stance phase. The results are compared with motor output records of the locust and with earlier force-plate measurements on the stick insect. It must be concluded that the mesothoracic leg initially resists forward movement of the body by the other legs during a typical walking step.     

Kinematics of walking in the hermit crab,Pagurus pollicarus

Hermit crabs are decapod crustaceans that have adapted to life in gastropod shells. Among their adaptations are modifications to their thoracic appendages or pereopods. The 4th and 5th pairs are adapted for shell support; walking is performed with the 2nd and 3rd pereopods, with an alternation of diagonal pairs. During stance, the walking legs are rotated backwards in the pitch plane. Two patterns of walking were studied to compare them with walking patterns described for other decapods, a lateral gait, similar to that in many brachyurans, and a forward gait resembling macruran walking.Video sequences of free walking and restrained animals were used to obtain leg segment positions from which joint angles were calculated. Leading legs in a lateral walk generated a power stroke by flexion of MC and PD joints; CB angles often did not change during slow walks. Trailing legs exhibited extension of MC and PD with a slight levation of CB. The two joints, B/IM and CP, are aligned at 90° angles to CB, MC and PD, moving dorso-anteriorly during swing and ventro-posteriorly during stance. A forward step was more complex; during swing the leg was rotated forward (yaw) and vertically (pitch), due to the action of TC. At the beginning of stance, TC started to rotate posteriorly and laterally, CB was depressed, and MC flexed. As stance progressed and the leg was directed laterally, PD and MC extended, so that at the end of stance the dactyl tip was quite posterior. During walks of the animal out of its shell, the legs were extended more anterior-laterally and the animal often toppled over, indicating that during walking in a shell its weight stabilized the animal.An open chain kinematic model in which each segment was approximated as a rectangular solid, the dimensions of which were derived from measurements on animals, was developed to estimate the CM of the animal under different load conditions. CM was normally quite anterior; removal of the chelipeds shifted it caudally. Application of forces simulating the weight of the shell on the 5th pereopods moved CM just anterior to the thoracic-abdominal junction. However, lateral and vertical coordinates were not altered under these different load conditions. The interaction of the shell aperture with proximal leg joints and with the CM indicates that the oblique angles of the legs, due primarily to the rotation of the TC joints, is an adaptation that confers stability during walking.     

Rotational locomotion by the cockroach Blattella germanica

Locomotion on complex substrata can be expressed in a plane by two geometric components of body movement: linear locomotion and rotational locomotion. This study examined pure rotation by analysing the geometry of leg movements and stepping patterns during the courtship turns of male Blattella germanica. Strict rotation or translation by an insect requires that each side of the body cover equal distance with respect to the substrate. There are three mechanisms by which the legs can maintain this equality: frequency of stepping, magnitude of the leg arcs relative to the body and the degree to which legs flex and extend during locomotion. During the courtship behaviour of Blattella germanica selected males executed turns involving body rotation along with leg movements in which the legs on the outside of the turn swung through greater average arcs than those on the inside of the turn. This difference should have resulted in a translation component. However, legs on the inside of the turn compensated by flexion and extension movements which were greater than those of opposing legs. The net effect was that both sides of the body covered equal average ground. These cockroaches used a wide variety of stepping combinations to effect rotation. The frequency of these combinations was compared to an expected frequency distribution of stepping combinations and further to an expected frequency of these stepping combinations used for straight walking. These comparisons demonstrated a similarity between interleg coordination during straight walking and that during turning in place.     

Interaction of central and peripheral mechanisms during walking in first instar stick insects, Extatosoma tiaratum

ABSTRACT. Individual stick insects were studied walking on a tread-wheel. When a leg caught hold of a small fixed rod beside the wheel it: (a) applied a rhythmically modulated backward directed force (with the modulation frequency identical to the stepping frequency of the other legs); or (b) regularly lifted off the stick during the phase of minimum force, and then returned to the stick; or (c) it stepped onto the wheel. If the wheel was stopped, the applied force increased. It is deduced that this behaviour is driven by central rhythmicity of unknown origin. All the known sensory inputs to this behaviour are superimposed on this central oscillation. A hypothesis is discussed which qualitatively fits all the experimental results on the effect of these sensory influences on the timing of an individual leg's movements in stick insects.     

The effects of sloped surfaces on locomotion: backward walking as a perturbation

The purpose of this study was to examine lower extremity kinetics and muscle activity during backward slope walking to clarify the relationship between joint moments and powers and muscle activity patterns observed in forward slope walking. Nine healthy volunteers walked backward on an instrumented ramp at three grades (-39% (-21 degrees ), 0% (level), +39% (+21 degrees )). EMG activity was recorded from major lower extremity muscles. Joint kinetics were obtained from kinematic and force platform data. The knee joint moment and power generation increased significantly during upslope walking; hip joint moment and power absorption increased significantly during downslope walking. When compared to data from forward slope walking, these backward walking data suggest that power requirements of a task dictate the muscle activity pattern needed to accomplish that movement. During downslope walking tasks, power absorption increased and changes in muscle activity patterns were directly related to the changes in the joint moment patterns. In contrast, during upslope walking tasks, power generation increased and changes in the muscle activity were related to the changes in the joint moments only at the 'primary' joint; at adjacent joints the changes in muscle activity were unrelated to the joint moment pattern. The 'paradoxical' changes in the muscle activity at the adjacent joints are possibly related to the activation of biarticular muscles required by the increased power generation at the primary joint. In total, these data suggest that changing power requirements at a joint impact the control of muscle activity at that and adjacent joints.     

Effects of circum-oesophageal lesion on the behaviour of the stick insect Carausius morosus

The co-ordination of the walking behaviour of decerebrate stick insects is examined and compared with normal behaviour. The walks are fully coordinated but undergo subtle changes in timing, have a longer average step period and show momentary pauses of 50 ms during the time course of protraction movements. In addition a new intersegmental reflex has been discovered. This tactile reflex is used to avoid errors in co-ordination that would be produced by posterior legs stepping onto the tarsi of the legs in front. The reflex has a latency of 100 ms and is easily observed in lesioned animals but is also active, although seldom seen, in slowly walking intact animals.     

Resonant frequencies of arms and legs identify different walking patterns

The present study is aimed at investigating changes in the coordination of arm and leg movements in young healthy subjects. It was hypothesized that with changes in walking velocity there is a change in frequency and phase coupling between the arms and the legs. In addition, it was hypothesized that the preferred frequencies of the different coordination patterns can be predicted on the basis of the resonant frequencies of arms and legs with a simple pendulum model. The kinematics of arms and legs during treadmill walking in seven healthy subjects were recorded with accelerometers in the sagittal plane at a wide range of different velocities (i.e., 0.3-1. 3m/s). Power spectral analyses revealed a statistically significant change in the frequency relation between arms and legs, i.e., within the velocity range 0.3-0.7m/s arm movement frequencies were dominantly synchronized with the step frequency, whereas from 0.8m/s onwards arm frequencies were locked onto stride frequency. Significant effects of walking speed on mean relative phase between leg and arm movements were found. All limb pairs showed a significantly more stable coordination pattern from 0.8 to 1.0m/s onwards. Results from the pendulum modelling demonstrated that for most subjects at low-velocity preferred movement frequencies of the arms are predicted by the resonant frequencies of individual arms (about 0.98Hz), whereas at higher velocities these are predicted on the basis of the resonant frequencies of the individual legs (about 0.85Hz). The results support the above-mentioned hypotheses, and suggest that different patterns of coordination, as shown by changes in frequency coupling and phase relations, can exist within the human walking mode.     

Two biomechanical strategies for locomotor adaptation to split-belt treadmill walking in subjects with and without transtibial amputation

Locomotor adaptation is commonly studied using split-belt treadmill walking, in which each foot is placed on a belt moving at a different speed. As subjects adapt to split-belt walking, they reduce metabolic power, but the biomechanical mechanism behind this improved efficiency is unknown. Analyzing mechanical work performed by the legs and joints during split-belt adaptation could reveal this mechanism. Because ankle work in the step-to-step transition is more efficient than hip work, we hypothesized that control subjects would reduce hip work on the fast belt and increase ankle work during the step-to-step transition as they adapted. We further hypothesized that subjects with unilateral, trans-tibial amputation would instead increase propulsive work from their intact leg on the slow belt. Control subjects reduced hip work and shifted more ankle work to the step-to-step transition, supporting our hypothesis. Contrary to our second hypothesis, intact leg work, ankle work and hip work in amputees were unchanged during adaptation. Furthermore, all subjects increased collisional energy loss on the fast belt, but did not increase propulsive work. This was possible because subjects moved further backward during fast leg single support in late adaptation than in early adaptation, compensating by reducing backward movement in slow leg single support. In summary, subjects used two strategies to improve mechanical efficiency in split-belt walking adaptation: a CoM displacement strategy that allows for less forward propulsion on the fast belt; and, an ankle timing strategy that allows efficient ankle work in the step-to-step transition to increase while reducing inefficient hip work.     

Mechanisms of stick insect locomotion in a gap-crossing paradigm

Locomotion of stick insects climbing over gaps of more than twice their step length has proved to be a useful paradigm to investigate how locomotor behaviour is adapted to external conditions. In this study, swing amplitudes and extreme positions of single steps from gap-crossing sequences have been analysed and compared to corresponding parameters of undisturbed walking. We show that adaptations of the basic mechanisms concern movements of single legs as well as the coordination between the legs. Slowing down of stance velocity, searching movements of legs in protraction and the generation of short steps are crucial prerequisites in the gap-crossing task. The rules of leg coordination described for stick insect walking seem to be modified, and load on the supporting legs is assumed to have a major effect on coordination especially in slow walking. Stepping into the gap with a front leg and antennal contact with the far edge of the gap provide information, as both events influence the following leg movements, whereas antennal non-contact seems not to contain information. Integration of these results into the model of the walking controller can improve our understanding of insect locomotion in highly irregular environments.Abbreviations AEP anterior extreme position - fAEP fictive anterior extreme position - PEP posterior extreme position - TOT treading-on-tarsus     

Individual differences and variability in the timing of motor activity during walking in insects

The uniformity of the neural physiology of an animal population is a fundamental, rarely tested assumption in most neurophysiological work. In this study, the variability of the timing between the movements of pairs of legs during free walking in cockroaches was assessed. Phases (a measure of timing) of motor bursts in muscles of legs in the American cockroach, Periplaneta americana, were calculated for insects walking straight over a flat, level surface. Student's t, Wallraff, Mann Whitney and Watson U² two-sample tests were used to compare the phases of motor bursts of the same pairs of legs in different insects. The comparisons showed that in spite of the homogeneity both of the animal population and of the conditions under which the insects walked, most of the inter-leg phases of the animals that were compared were significantly different statistically. Further testing of greater numbers of insects using analysis of variance to test for population uniformity confirmed that the insects we tested were not members of a single statistical population with respect to the timing of motor bursts of the legs during walking. We infer that this unexpectedly large variability in a population thought to be relatively homogeneous reflects subtle but biologically significant differences between animals. The possible sources of these differences and their consequences for the study of behavior and its physiological basis are discussed.     

Kinematics and motor activity during tethered walking and turning in the cockroach, <Emphasis Type="Italic">Blaberus discoidalis</Emphasis>

When insects turn from walking straight, their legs have to follow different motor patterns. In order to examine such pattern change precisely, we stimulated single antenna of an insect, thereby initiating its turning behavior, tethered over a lightly oiled glass plate. The resulting behavior included asymmetrical movements of prothoracic and mesothoracic legs. The mesothoracic leg on the inside of the turn (in the apparent direction of turning) extended the coxa-trochanter and femur-tibia joints during swing rather than during stance as in walking, while the outside mesothoracic leg kept a slow walking pattern. Electromyograms in mesothoracic legs revealed consistent changes in the motor neuron activity controlling extension of the coxa-trochanter and femur-tibia joints. In tethered walking, depressor trochanter activity consistently preceded slow extensor tibia activity. This pattern was reversed in the inside mesothoracic leg during turning. Also for turning, extensor and depressor motor neurons of the inside legs were activated in swing phase instead of stance. Turning was also examined in free ranging animals. Although more variable, some trials resembled the pattern generated by tethered animals. The distinct inter-joint and inter-leg coordination between tethered turning and walking, therefore, provides a good model to further study the neural control of changing locomotion patterns.