Adaptive control for insect leg position: controller properties depend on substrate compliance

This paper concentrates on the system that controls the femur-tibia joint in the legs of the stick insect, Carausius morosus. Earlier investigations have shown that this joint is subject to a mixture of proportional and differential control whereby the differential part plays a prominent role. Experiments presented here suggest another interpretation: single legs of a stick insect were systematically perturbed using devices of different compliance and compensatory forces and movements monitored. When the compliance is high (soft spring), forces are generated that return the leg close to its original position. When the compliance is low (stiff spring), larger forces are generated but sustained changes in position occur that are proportional to the force that is applied. Selective ablation of leg sense organs showed that the leg did not maintain its position after elimination of afferents of the femoral chordotonal organ. Ablation of leg campaniform sensilla had no effect. These data support the idea that different control strategies are used, depending upon substrate compliance. In particular, what we and other authors have called a differential controller, is now considered as an integral controller that intelligently gives up when the correlation between motor output and movement of the leg is low.We would like to dedicate this article to Prof. Dr. Ulrich Bässler. Starting in the 1960s, his seminal work stimulated a long series of fruitful studies that, even today, reveal exciting insights into motor control.     

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     

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.     

Sensing the effect of body load in legs: responses of tibial campaniform sensilla to forces applied to the thorax in freely standing cockroaches

Sense organs in the legs that detect body weight are an important component in the regulation of posture and locomotion. We tested the abilities of tibial campaniform sensilla, receptors that can monitor forces in the cockroach leg, to encode variations in body load in freely standing animals. Small magnets were attached to the thorax and currents were applied to a coil below the substrate. Sensory and motor activities were monitored neurographically. The tibial sensilla could show vigorous discharges to changing forces when animals stood upon their legs and actively supported the body weight. Firing of individual afferents depended upon the orientation of the receptors cuticular cap: proximal sensilla (oriented perpendicular to the leg axis) discharged to force increases while distal receptors (parallel to the leg) fired to decreasing forces. Proximal sensillum discharges were prolonged and could encode the level of load when increases were sustained. Firing of the trochanteral extensor motoneuron was also strongly modulated by changing load. In some postures, sensillum discharges paralleled changes in motor frequency consistent with a known interjoint reflex. These findings demonstrate that tibial campaniform sensilla can monitor the effects of body weight upon the legs and may aid in generating support of body load.     

Behaviorally significant immobile state of so-called thanatosis in the cricket Gryllus bimaculatus DeGeer: its characterization, sensory mechanism and function

We have found that the cricket Gryllus bimaculatus shows an immobile posture, so-called thanatosis. Thanatosis was reflexly elicited by gently holding the forelegs and pronotum of the cricket. During thanatosis, the respiration rate decreased markedly while the heart rate doubled compared with the resting state. Animals in the state of extreme rigidity were unresponsive to the external disturbances but easily aroused by mechanical stimulation such as prodding. The immobile posture usually persisted for 2–4 min, but occasionally for more than 20 min, and then suddenly ended. Catalepsy was induced during thanatosis when a leg was passively forced to the extended position. For elicitation of the flexion reflex, either campaniform sensilla and femoral chordotonal organs (FCOs) in the forelegs, and spine-like sensilla on the pronotum were necessary. Among these receptors, however, only the FCOs were involved in inducing the immobile state. Centrally, the brain was indispensable for thanatosis to be maintained. In semi-natural conditions the thanatotic state did occur spontaneously while the cricket struggled to get into a small crevice according to the nature of this species. This sudden immobilization could help the cricket get out of danger of predators like reptiles and amphibians in the natural habitat.Abbreviations FCO femoral chordotonal organ - F-T femorotibial - N nerve     

Anatomy and physiology of trochanteral campaniform sensilla in the stick insect, Cuniculina impigra

ABSTRACT. Four groups of campaniform sensilla are found on the trochanter of Cuniculina impigra Tedtenbacher (Phasmidae). One of these groups can be divided into two sub-groups. The sensilla are approximately parallel within each group or sub-group. As sensilla with parallel orientation will respond to the same direction of shear force, each group or sub-group of campaniform sensilla should act as one unit. When the coxa is fixed, activity in the nerve supplying the campaniform sensilla can be released by bending the femur forwards and backwards. The sensilla are sensitive to movement only in one direction. The investigated sensilla react to the stimulus with phasic-tonic discharge patterns. The dependence of the phasic component upon the velocity of the stimulus can be described by a power function. The tonic component depends on the amplitude of the stimulus. By mechanical stimulation of individual groups of sensilla it can be shown that at least two groups of campaniform sensilla contain units which respond to bending the femur backwards. The activity of some motor neurones can be influenced by slightly bending the leg in the horizontal plane. The levator trochanteris muscle is activated when the femur is bent forwards, and the frequency of the slow extensor tibiae motor neurone is increased when the femur is bent backwards. The reaction of both muscles is phasic. There is no detectable reaction in the protractor or the retractor of the coxa or the depressor trochanteris.     

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.     

Dynamic responses of tibial campaniform sensilla studied by substrate displacement in freely moving cockroaches

Responses of the tibial campaniform sensilla, receptors that encode strains in the exoskeleton, were characterized by recording sensory activities during perturbations in freely standing cockroaches. The substrate upon which the animal stood was displaced horizontally using ramp and hold stimuli at varied rates. The sensilla showed short latency responses that were initiated in the first 30 ms of platform movement. Responses of individual receptors depended upon the direction of displacement and the orientation of their cuticular cap. Proximal receptors, whose caps are perpendicular to the long axis of the tibia, responded to displacements directed from the contralateral side of the body and from the head toward the abdomen. The distal sensilla, oriented parallel to the tibia, discharged at longer latency to displacements in opposite directions. Plots of receptor activity versus displacement direction showed that proximal and distal sensilla are activated in non-overlapping ranges of movement direction. Afferent responses also increased as the platform was displaced more rapidly. These results are consistent with a model in which displacements produce forces that result in bending of the tibia. This information could be utilized to detect the direction and rate of forces that occur during leg slipping or in walking on unstable terrains.     

The walking-(and searching-) pattern generator of stick insects,a modular system composed of reflex chains and endogenous oscillators

Stick insects (Cuniculina impigra) possessing only one front leg with restrained coxa performed searching movements or walked on a treadband. The movements are described. Ablation, surgical manipulation or experimental stimulation of different sense organs (femoral chordotonal organ, campaniform sensilla on trochanter and femur basis, proprioceptors at the coxatrochanter joint) were performed, and the resulting changes in motor output were recorded. These experiments demonstrate that the walking- and searching-pattern generators cannot be separated, at least not for the movements investigated. This walking- and searching-pattern generator consists of central modules, each of which produces irregular alternation of the activity of motor neurones of antagonistic muscles of a single joint, and of reflex loops. At least some of these reflex loops are only present in the active animal. They are responsible either for the control of a single joint or for the coordination of the movements of separate joints. The performance of these reflexes does not only depend on the state of activity of the animal; some of them additionally seem to depend on the context signalled by other sense organs.     

The network producing the “active reaction” of stick insects is a functional element of different pattern generating systems

Elongation of the femoral chordotonal organ (signalling a flexion movement of the femur-tibia joint) in stick insects being active releases the active reaction (AR) in the extensor and flexor motor neurones. The AR was released in hindlegs in a situation where free animals would preferentially walk backwards. In most cases the coordination between extensor-flexor and the retractor unguis muscle was like in a stance phase of backward walking. In a situation where free animals would preferentially walk forwards, the percentage of ARs was smaller, and resistance reflexes became more frequent. When campaniform sensilla of the hind leg were destroyed coordinations like in a swing phase of forward walking became more frequent. — Additional stimuli during searching movements in an artificially closed femur-tibia feedback system (Weiland et al. 1986) showed that the AR is expressed also under these conditions and controls velocity and endpoint of a flexion movement. All results support the idea that the neural system producing the AR is a functional element of the pattern generator for forward walking, of the one for backward walking and of the one for searching movements. As far as this system is concerned the three pattern generators only differ in the kind of coordinating pathways between constant functional elements.     

Adaptive reconfiguration of a reflex circuit during different motor programmes in the locust

The cuticle strain which develops in the hindleg tibiae when a locust prepares to kick, or when the tibia thrusts against an obstacle, is detected by two campaniform sensilla, which reflexly excite the fast extensor tibiae motoneuron, some of the flexor tibiae motoneurons and nonspiking interneurons. The reflex excitation is adaptive for the extensor motoneuron during both co-activation and thrusting, but is only adaptive for the flexor motoneurons during co-activation, and is maladaptive during thrusting. We show that the femoral chordotonal organ, which monitors tibial position, controls the efficacy of the strain feedback. The campaniform sensilla-induced depolarization in the extensor motoneuron is about twice as large when the tendon is in mid position (reflecting a tibial-femoral angle of 90°) than when fully stretched (reflecting tibial flexion), while in the flexors the reverse is true. The amplitudes of excitatory postsynaptic potentials evoked by single campaniform sensilla spikes, are, however, not affected. Our data suggests that the chordotonal organ modulates the gain of the strain feedback onto the motoneurons by exciting interneuronal circuits whose output sums with the former. Thrusting typically occurs with the tibia partially extended, therefore the actions of the chordotonal organ support the production of a maximal thrusting force. Accepted: 27 December 1996     

Tuning posture to body load: decreases in load produce discrete sensory signals in the legs of freely standing cockroaches

Decreases in load are important cues in the control of posture and walking. We recorded activities of the tibial campaniform sensilla, receptors that monitor forces as strains in the exoskeleton, in the middle legs of freely moving cockroaches. Small magnets were attached to the thorax and body load was changed by applying currents to a coil below the substrate. Body position was monitored by video recording. The tibial sensilla are organized into proximal and distal subgroups that have different response properties and reflex effects: proximal sensilla excite extensor motoneurons while distal receptors inhibit extensor firing. Sudden load decreases elicited bursts from distal sensilla, while increased load excited proximal receptors. The onset of sensory discharges closely approximated the time of peak velocity of body movement in both load decreases and increases. Firing of distal sensilla rapidly adapted to sustained unloading, while proximal sensilla discharged tonically to load increases. Load decreases of small amplitude or at low rates produced only inhibition of proximal activity while decrements of larger size or rate elicited distal firing. These response properties may provide discrete signals that either modulate excitatory extensor drive during small load variations or inhibit support prior to compensatory stepping or initiation of swing.     

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.     

Identified nonspiking interneurons in leg reflexes and during walking in the stick insect

In the stick insect Carausius morosus identified nonspiking interneurons (type E4) were investigated in the mesothoracic ganglion during intraand intersegmental reflexes and during searching and walking.In the standing and in the actively moving animal interneurons of type E4 drive the excitatory extensor tibiae motoneurons, up to four excitatory protractor coxae motoneurons, and the common inhibitor 1 motoneuron (Figs. 1–4).In the standing animal a depolarization of this type of interneuron is induced by tactile stimuli to the tarsi of the ipsilateral front, middle and hind legs (Fig. 5). This response precedes and accompanies the observed activation of the affected middle leg motoneurons. The same is true when compensatory leg placement reflexes are elicited by tactile stimuli given to the tarsi of the legs (Fig. 6).During forward walking the membrane potential of interneurons of type E4 is strongly modulated in the step-cycle (Figs.8–10). The peak depolarization occurs at the transition from stance to swing. The oscillations in membrane potential are correlated with the activity profile of the extensor motoneurons and the common inhibitor 1 (Fig. 9).The described properties of interneuron type E4 in the actively behaving animal show that these interneurons are involved in the organization and coordination of the motor output of the proximal leg joints during reflex movements and during walking.Abbreviations CLP reflex, compensatory leg placement reflex - CI1 common inhibitor I motoneuron - fCO femoral chordotonal organ - FETi fast extensor tibiae motoneuron - FT femur-tibia - SETi slow extensor tibiae motoneuron     

Campaniform sensilla of Calliphora vicina (Insecta,Diptera)

Summary A classification scheme of campaniform sensilla using morphological criteria was developed. All variations of the two most important outer structural elements, the cuticular cap and the cuticular collar, were taken into consideration: (a) the external shape of the cuticular cap; (b) the position of the cuticular cap in relation to the remaining cuticle; (c) the position of the cuticular collar in relation to the cuticular cap. This resulted in a classification of campaniform sensilla into 24 types. This typology was applied to the campaniform sensilla of Calliphora, which show considerable variations in their outer structures. According to SEM (scanning electron microscope) pictures and TEM (transmission electron microscope) sections we found only 9 out of 24 different types of campaniform sensilla in the fly.     

Force detection in cockroach walking reconsidered: discharges of proximal tibial campaniform sensilla when body load is altered

We examined the mechanisms underlying force feedback in cockroach walking by recording sensory and motor activities in freely moving animals under varied load conditions. Tibial campaniform sensilla monitor forces in the leg via strains in the exoskeleton. A subgroup (proximal receptors) discharge in the stance phase of walking. This activity has been thought to result from leg loading derived from body mass. We compared sensory activities when animals walked freely in an arena or on an oiled glass plate with their body weight supported. The plate was oriented either horizontally (70-75% of body weight supported) or vertically (with the gravitational vector parallel to the substrate). Proximal sensilla discharged following the onset of stance in all load conditions. In addition, activity was decreased in the middle third of the stance phase when the effect of body weight was reduced. Our results suggest that sensory discharges early in stance result from forces generated by contractions of muscles that press the leg as a lever against the substrate. These forces can unload legs already in stance and assure the smooth transition of support among the limbs. Force feedback later in stance may adjust motor output to changes in leg loading.     

The development of the sensory organs of the legs in the blowfly,Phormia regina

Summary The development of the sensory neurons of the legs of the blowfly,Phormia regina has been described from the third instar larva to the late pupa using immunohistochemical staining. The leg discs of the third instar larva contain 8 neurons of which 5 come to lie in the fifth tarsomere of the developing leg. Whereas 2 neurons persist at least to the late pupa, the other cells degenerate. The first neurons of gustatory sensilla arise in the fifth tarsomere at about 1.5 h after formation of the puparium. Most of these sensilla, however, appear within a short time period beginning at about 18 h. The femoral chordotonal sensory neurons first appear at the time of formation of the puparium, as a mass of cells situated in the distal femur. During later pupal development 2 groups of these cells come to lie at the femur-trochanter border, where they become the proximal femoral chordotonal organ of the adult; the remaining cells become the distal femoral chordotonal organ. Other scolopidial neurons appear later in development. The nerve pathways of the late pupal leg are established either by the axons of the cells that are present in the larval leg disc or by new outgrowing processes of sensory neurons. In the tibia, the initial direction of new outgrowth differs in different regions of the segment: proximal tibial neurons grow distally, while distal tibial neurons grow initially proximally.     

The fine structure of the cockroach subgenual organ

This paper describes the fine structure of the cockroach subgenual organ, a complex ciliated mechanoreceptor that detects vibrations in the substrate upon which the animal stands. Located beneath the knee in each walking leg, the cockroach subgenual organ is a thin, fan-shaped flap of tissue slung across the dorsal blood space of the tibia at right angles to the leg's long axis. It is innervated by approximately 50 chordotonal sensilla. The fine structure of the chordotonal sensilla is is described in detail ; possible transducer sites are discussed.     

The central connections and actions during walking of tibial campaniform sensilla in the locust

Strain acting on the exoskeleton of insects is monitored by campaniform sensilla. On the tibia of a mesothoracic leg of the locust (Schistocerca gregaria) there are three groups of campaniform sensilla on the proximo-dorsal surface. This study analyses the responses of the afferents from one group, their connections with central neurones and their actions during walking.The afferents of the campaniform sensilla make direct excitatory connections with flexor tibiae motor neurones. They also make direct connections with particular spiking local interneurones that make direct inhibitory output connections with the slow extensor tibiae motor neurone.During walking extension movements of the tibiae during stance produce longitudinal tensile forces on the dorsal tibia that peak during mid stance before returning to zero prior to swing. This decline in tension can activate the campaniform sensilla. In turn this would lead to an inhibition of the extensor tibiae motor neurone and an excitation of the flexor tibiae motor neurones. This, therefore, aids the transition from stance to swing. During turning movements, the tibia is flexed and the dorsal surface is put under compression. This can also activate some of campaniform sensilla whose effect on the flexor motor neurones will reinforce the flexion of the tibia.     

Zur Beeinflussung der Bewegungsweise eines Beines von Carausius morosus durch Amputation anderer Beine

Amputation of a leg alters the amplitude of the adjacent ipsilateral legs during walking: Amputation of a middle leg encreases the amplitude of the foreleg especially by changing the rear extreme position. Amputation of a foreleg reduces the amplitude of the middle leg especially by changing the front extreme position. There is no significant influence observable on contralateral legs.