Sensory control of leg movement in the stick insect Carausius morosus

Hind legs with crossed receptor-apodemes of the femoral chordotonal organ when making a step during walking often do not release the ground after reaching the extreme posterior position. After putting a clamp on the trochanter (stimulation of the campaniform sensilla) the leg is no longer protracted during walking. However, during searching-movements the same leg is moved very far forwards. The anatomical situation of the campaniform sensilla on the trochanter and the sensory innervation of the trochanter is described. After removal of the hair-rows and continuously stimulating the hair-plate at the thorax-coxa-joint the extreme anterior and posterior positions of the leg in walking are displaced in the posterior direction. Front and middle legs operated in this way sometimes do not release the ground at the end of retraction. In searching-movements the same leg is moved in a normal way. If only one side of a decerebrated animal goes over a step, then on the other side a compensatory effect is observed. The main source of this compensatory information appears to be the BF1-hair-plates. If the animal has to drag a weight the extreme anterior and posterior positions of the middle and hind legs are displaced in the anterior direction. Crossing the receptor-apodeme of the femoral chordotonal organ, when it causes the leg to remain in the protraction phase, displaces the extreme posterior position of the ipsilateral leg in front of the operated one in the posterior direction. Influences of different sources on the extreme posterior position can superimpose. A model is presented which combines both a central programme and peripheral sensory influence. The word programme used here means that it does not only determine the motor output but also determines the reactions to particular afferences. The fact that the reaction to a stimulus depends on the internal state of the CNS is also represented by the model.Supported by Deutsche Forschungsgemeinschaft     

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.     

Leg movements of stick insects walking with five legs on a treadwheel and with one leg on a motor-driven belt

Five legs of a fixed stick insect walked on a double treadwheel. The left hindleg (L3) walked on a motor-driven belt. When the belt was slower than the wheels L3 made less steps than the other legs and when the belt was faster than the wheels it made more steps than the other legs. In the case of slowlier stepping of the belt-leg, the motor neurons of the retractor coxae muscle of this leg showed a high activity when the leg was pulled backwards by the belt. This activity was modulated in the step rhythm of the wheel-legs. When all legs showed the same stepping frequency (1:1-coordination) the protraction duration of L3 was almost independent of step-period, as well as the lag between onset of protraction of L3 and that of L2. In some cases only L3 could be made to step on the belt even when all other legs did not walk.     

Vom femoralen Chordotonalorgan gesteuerte Reaktionen bei der Stabheuschrecke Carausius morosus: Messung der von der Tibia erzeugten Kraft im aktiven und inaktiven Tier

In the Introduction (A) there is a list of unsolved problems concerning the role of the femoral chordotonal organ. A method to solve these problems by measuring the force at the distal end of the tibia during stimulation of the femoral chordotonal organ is described in (B). The step-response in inactive animals (C) is similar to that of the free-moving tibia. After an active movement caused by touching the abdomen the amplitude of the flexion-force is always higher than before. In (D) a method is described to measure the amplification of the control-system in intact animals. With this method it is verified, that the flexion-force produced by a distinct stimulus is higher after active movements caused by touching the abdomen. But this force is lower after spontaneous active movements caused by darkening the room (Fig. 2). Therefore one must assume, that there are two different types of activity: spontaneous activity and activity after a disturbance. In the frequency-response of the inactive animal (F) (Figs. 4 and 5) the amplitude of the force decreases with increasing frequency at a constant amplitude of stimulus. The phase-shift between reaction and stimulus is much smaller than with the free-moving tibia. Therefore, the large phase-shift as well as the strong decrease of the reaction-amplitude near 1 Hz observed in free-moving tibias (1972b) is mainly due to the mechanical attributes of the system. In Section (F) the receptor-apodeme is sinusoidally moved during active movements of intact and decerebrated animals. As with the free-moving tibia no reaction can be observed during active movements at that phase position for which the response occurs in inactive animals. Instead of this inactive response there is another response, called active with a phase-shift of about 180°. At the end of an active period the active and the inactive response can be observed simultaneously (Figs. 7 and 10). The amplitude of the active response decreases, and the amplitude of the inactive response increases from cycle to cycle. In decerebrated animals there are normally several minutes from the exclusively active response to the exclusively inactive response without a further increase in amplitude. In intact animals this transition takes only a few seconds. Step-stimuli during active movements (G) show, that in active animals stretching the chordotonal organ causes a flexion of the femor-tibia-joint. Releasing the chordotonal organ does not produce any reaction. Moving the receptor-apodeme in active animals influences the contralateral leg significantly only in middle legs (H). These legs tend to move within the same phase position as the stimulated leg. Moving the receptor-apodeme in a middle leg has no influence on the ipsilateral hind leg, but a weak influence on the ipsilateral front leg, which tends to move within the same phase position as the middle leg. In the discussion (I) a hypothesis is presented according to which the active response is a mechanism for adapting the leg movement to a surface which suddenly gives way (I 5). The influence on the contralateral middle leg seems to be a part of this mechanism (I 6). This reaction has nothing to do with the coordination of leg movements in walk (I 7). The feed-back systems which control the distance between the body and the walking surface may be inactive during walking (I 8), but those systems which control the forward movement of the body must be active. Since the feed-back system of the Kniesehnen-reflex controls predominantly the body-ground-distance it seems likely that it is normally inactive during walking.     

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.     

Oscillations of force in the standing legs of a walking insect (Carausius morosus)

In the experiments presented here adult stick insects (Carausius morosus) walk on a treadwheel with various legs standing on platforms fixed relative to the body of the insect. These standing legs produce large forees directed towards the rear which are modulated in the rhythm of the walking legs. Neighbouring legs which both stand on a platform often oscillate in phase. Possible reasons for the occurrence of the force oscillations are discussed.Supported by DFG (Cr 58/1)     

The antennal motor system of the stick insect Carausius morosus: anatomy and antennal movement pattern during walking

The stick insect Carausius morosus continuously moves its antennae during locomotion. Active antennal movements may reflect employment of antennae as tactile probes. Therefore, this study treats two basic aspects of the antennal motor system: First, the anatomy of antennal joints, muscles, nerves and motoneurons is described and discussed in comparison with other species. Second, the typical movement pattern of the antennae is analysed, and its spatio-temporal coordination with leg movements described. Each antenna is moved by two single-axis hinge joints. The proximal head-scape joint is controlled by two levator muscles and a three-partite depressor muscle. The distal scape-pedicel joint is controlled by an antagonistic abductor/ adductor pair. Three nerves innervate the antennal musculature, containing axons of 14-17 motoneurons, including one common inhibitor. During walking, the pattern of antennal movement is rhythmic and spatiotemporally coupled with leg movements. The antennal abduction/adduction cycle leads the protraction/retraction cycle of the ipsilateral front leg with a stable phase shift. During one abduction/adduction cycle there are typically two levation/depression cycles, however, with less strict temporal coupling than the horizontal component. Predictions of antennal contacts with square obstacles to occur before leg contacts match behavioural performance, indicating a potential role of active antennal movements in obstacle detection.     

Active tactile exploration for adaptive locomotion in the stick insect

Insects carry a pair of actively movable feelers that supply the animal with a range of multimodal information. The antennae of the stick insect Carausius morosus are straight and of nearly the same length as the legs, making them ideal probes for near-range exploration. Indeed, stick insects, like many other insects, use antennal contact information for the adaptive control of locomotion, for example, in climbing. Moreover, the active exploratory movement pattern of the antennae is context-dependent. The first objective of the present study is to reveal the significance of antennal contact information for the efficient initiation of climbing. This is done by means of kinematic analysis of freely walking animals as they undergo a tactually elicited transition from walking to climbing. The main findings are that fast, tactually elicited re-targeting movements may occur during an ongoing swing movement, and that the height of the last antennal contact prior to leg contact largely predicts the height of the first leg contact. The second objective is to understand the context-dependent adaptation of the antennal movement pattern in response to tactile contact. We show that the cycle frequency of both antennal joints increases after obstacle contact. Furthermore, inter-joint coupling switches distinctly upon tactile contact, revealing a simple mechanism for context-dependent adaptation.     

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.     

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.