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.     

Tight turns in stick insects

We investigated insects Carausius morosus walking whilst hanging upside down along a narrow 3 mm horizontal beam. At the end of the beam, the animal takes a 180° turn. This is a difficult situation because substrate area is small and moves relative to the body during the turn. We investigated how leg movements are organised during this turn. A non-contact of either front leg appears to indicate the end of the beam. However, a turn can only begin if the hind legs stand in an appropriate position relative to each other; the outer hind leg must not be placed posterior to the inner hind leg. When starting the turn, both front legs are lifted and usually held in a relatively stable position and then the inner middle leg performs a swing-and-search movement: The leg begins a swing, which is continued by a searching movement to the side and to the rear, and eventually grasps the beam. At the same time the body is turned usually being supported by the outer middle leg and both hind legs. Then front legs followed by the outer middle leg reach the beam. A scheme describing the turns based on a few simple behavioural elements is proposed.     

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.     

Reflex modulation in locusts walking on a treadwheel intracellular recordings from motoneurons

Summary In locusts (Locusta migratoria) walking on a treadwheel, afferents of tarsal hair sensilla were stimulated via chronically implanted hook electrodes (Fig. 1). Stimuli applied to the middle leg tarsus elicited avoidance reflexes (Fig. 2). In quiescent animals, the leg was lifted off the ground and the femur adducted. In walking locusts, the response was phase-dependent. During the stance phase, no reaction was observed except occasional, premature triggering of swing movements; stimuli applied near the end of the swing phase were able to elicit an additional, short leg protraction.Central nervous correlates of phase-dependent reflex modulation were observed by recording intracellularly from motoneuron somata in walking animals. As a rule, motoneurons recruited during the swing phase showed excitatory stimulus-related responses around the end of the swing movement, correlated to the triggering of additional leg protractions (Figs. 3, 4, 5). Motoneurons active during the stance phase were often inhibited by tarsal stimulation, some showed only weak responses (Figs. 8, 9, 10). Common inhibitory motoneuron 1 was excited by tarsal stimulation during all phases of the leg movement (Figs. 6, 7). In one type of flexor tibiae motoneuron, a complex response pattern was observed, involving the inversion of stimulus-related synaptic potentials from excitatory, recorded during rest, to inhibitory, observed during long-lasting stance phases (Figs. 11, 12).The results demonstrate how reflex modulation is represented on the level of synaptic input to motoneurons. They further suggest independent gain control in parallel, antagonistic pathways converging onto the same motoneuron as a mechanism for reflex reversal during locomotion.Abbreviations CI ₁ common inhibitory motoneuron (1) - EMG electromyogram - Feti fast extensor muscle of the tibia     

Organization of a complex movement: fixed and variable components of the cockroach escape behavior

The escape behavior of the cockroach Periplaneta americana was studied by means of high speed filming (250 frames/s) and a computer-graphical analysis of the body and leg movements. The results are as follows: 1. The behavior begins with pure rotation of the body about the posteriorly located cerci, followed by rotation plus forward translation, and finally pure translation (Figs. 1, 2). 2. A consistent inter-leg coordination is used for the entire duration of the turn (Fig. 3A). At the start of the movement, five or all six legs execute their first stance phase (i.e. leg on the ground during locomotion) simultaneously. By the end of the turn the pattern has changed to the alternate 'tripod' coordination characteristic of insect walking. The change-over from all legs working together, to working alternately, occurs by means of a consistent pattern of delays in the stepping of certain legs. 3. The movements made by each leg during its initial stance phase are carried out using consistent movement components in the anterior-posterior (A-P) and the medial-lateral (M-L) axes (Fig. 4A). The movement at a particular joint in each middle leg is found to be diagnostic for the direction of turn. 4. The size and direction of a given leg's M-L movement in its initial stance phase depends on the same leg's prior A-P position (Fig. 5). No such feedback effects were seen among different legs. 5. Animals that are fixed to a slick surface on which they make slipping leg movements show the same inter-leg coordination (Fig. 3B), direction of initial stance movement (Fig. 4B) and dependence of the leg's initial M-L movement on its prior A-P position (Fig. 6), as did free-ranging animals. 6. Cockroaches that are walking at the moment they begin their escape reverse those ongoing leg movements that are contrary to escape movements. 7. These results are discussed in terms of the overall coordination of the complex movements, and in terms of the known properties of the neural circuitry for escape. Possibilities for neurobiological follow-up of certain of the findings presented here are also addressed.     

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.     

Interaction between descending input and thoracic reflexes for joint coordination in cockroach. II Comparative studies on tethered turning and searching

Tethered cockroaches turn from unilateral antennal contact using asymmetrical movements of mesothoracic (T2) legs (Mu and Ritzmannin J Comp Physiol A 191:1037–1054, 2005). During the turn, the leg on the inside of the turn (the inside T2 leg) has distinctly different motor patterns from those in straight walking. The transformation from walking to inside leg turning could be triggered by descending commands that alter a few critical reflexes that start a cascade of physical changes in leg movement or posture, leading to further alterations. This hypothesis has two implications: First, the descending activities must be able to influence thoracic reflexes. Second, one should be able to initiate the turning motor pattern in the absence of descending signals by mimicking a point farther down in the reflex cascade. We addressed the first implication in the companion paper. To examine the second implication, we compared kinematics and motor activities of the T2 leg during searching with that of inside leg turning. The reaching movements made during searching were found to be similar to the movements made by the inside leg during turning. Moreover, even after disconnecting the brain from the thoracic ganglia the reaching movements were similar. This observation is consistent with the second implication from the hypothesis.     

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.     

A bipedal compliant walking model generates periodic gait cycles with realistic swing dynamics

A simple spring mechanics model can capture the dynamics of the center of mass (CoM) during human walking, which is coordinated by multiple joints. This simple spring model, however, only describes the CoM during the stance phase, and the mechanics involved in the bipedality of the human gait are limited. In this study, a bipedal spring walking model was proposed to demonstrate the dynamics of bipedal walking, including swing dynamics followed by the step-to-step transition. The model consists of two springs with different stiffnesses and rest lengths representing the stance leg and swing leg. One end of each spring has a foot mass, and the other end is attached to the body mass. To induce a forward swing that matches the gait phase, a torsional hip joint spring was introduced at each leg. To reflect the active knee flexion for foot clearance, the rest length of the swing leg was set shorter than that of the stance leg, generating a discrete elastic restoring force. The number of model parameters was reduced by introducing dependencies among stiffness parameters. The proposed model generates periodic gaits with dynamics-driven step-to-step transitions and realistic swing dynamics. While preserving the mimicry of the CoM and ground reaction force (GRF) data at various gait speeds, the proposed model emulated the kinematics of the swing leg. This result implies that the dynamics of human walking generated by the actuations of multiple body segments is describable by a simple spring mechanics.     

Effects of load inversion in cockroach walking

To examine how walking patterns are adapted to changes in load, we recorded leg movements and muscle activities when cockroaches (Periplaneta americana) walked upright and on an inverted surface. Animals were videotaped to measure the hindleg femoro-tibial joint angle while myograms were taken from the tibial extensor and flexor muscles. The joint is rapidly flexed during swing and extended in stance in upright and inverted walking. When inverted, however, swing is shorter in duration and the joint traverses a range of angles further in extension. In slow upright walking, slow flexor motoneurons fire during swing and the slow extensor in stance, although a period of co-contraction occurs early in stance. In inverted walking, patterns of muscle activities are altered. Fast flexor motoneurons fire both in the swing phase and early in stance to support the body by pulling the animal toward the substrate. Extensor firing occurs late in stance to propel the animal forward. These findings are discussed within the context of a model in which stance is divided into an early support and subsequent propulsion phase. We also discuss how these changes in use of the hindleg may represent adaptations to the reversal of the effects of gravity.     

Walking in Aretaon asperrimus

This article describes basic parameters characterizing walking of the stick insect Aretaon asperrimus to allow a comparative approach with other insects studied. As in many other animals, geometrical parameters such as step amplitude and leg extreme positions do not vary with walking velocity. However, the relation between swing duration and stance duration is quite constant, in contrast to most insects studied. Therefore, velocity profiles during swing vary with walking velocity whereas time course of leg trajectories and leg angle trajectories are independent of walking velocity. Nevertheless, A. asperrimus does not show a classical tripod gait, but performs a metachronal, or tetrapod, gait, showing phase values differing from 0.5 between ipsilateral neighbouring legs. As in Carausius morosus, the detailed shape of the swing trajectory may depend on the form of the substrate. Effects describing coordinating influences between legs have been found that prevent the start of a swing as long as the posterior leg performs a swing. Further, the treading on tarsus reflex can be observed in Aretaon. No hint to the existence of a targeting influence has been found. Control of rearward walking is easiest interpreted by maintaining the basic rules but an anterior-posterior reversal of the information flow.     

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     

Common motor mechanisms support body load in serially homologous legs of cockroaches in posture and walking

We studied the mechanisms underlying support of body load in posture and walking in serially homologous legs of cockroaches. Activities of the trochanteral extensor muscle in the front or middle legs were recorded neurographically while animals were videotaped. Body load was increased via magnets attached to the thorax and varied through a coil below the substrate. In posture, tonic firing of the slow trochanteral extensor motoneuron (Ds) in each leg was strongly modulated by changing body load. Rapid load increases produced decreases in body height and sharp increments in extensor firing. The peak of extensor activity more closely approximated the maximum velocity of body displacement than the body position. In walking, extensor bursts in front and middle legs were initiated during swing and continued into the stance phase. Moderate tonic increases in body load elicited similar, specific, phase dependent changes in both legs: extensor firing was not altered in swing but was higher after foot placement in stance. These motor adjustments to load are not anticipatory but apparently depend upon sensory feedback. These data are consistent with previous findings in the hind legs and support the idea that body load is countered by common motor mechanisms in serially homologous legs.     

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     

Phase-Dependent Effects of Transcutaneous Spinal Cord Stimulation on Regulation of Kinematics of Human Stepping Motions

The effect of transcutaneous electrical spinal cord stimulation on the kinematic parameters of movement of the ipsilateral and contralateral legs in healthy subjects during treadmill walking at speeds of 1.5 to 1.7 km/h has been studied. The stimulation electrodes were placed 2.5 cm lateral from the right and left sides of the spinal midline at L1 and T11 levels. During the stance phase, stimulation was administered at L1 level at a frequency of 15 Hz; during the swing phase the stimuli was delivered to T11 at a frequency of 30 Hz, followed by alternating stimulation at L1 and T11. The stimulation during the swing phase (T11) was more effective than that during the stance phase (L1); the most impressive changes in kinematic parameters were observed when combined delivery of stimulations to L1 and T11 was performed. With unilateral spinal stimulation, the amplitude of the angles in the hip, knee and/or ankle joints, the length of the transfer, and the height of the leg elevation increased in the ipsilateral leg. Similar but less pronounced changes were observed in the contralateral leg. A 10% increase in the duration of stimulation in the swing phase caused a change in the kinematic stepping parameters both in ipsilateral and contralateral legs. The maximum effect was observed when bilateral alternating stimulation was used. These data show that phasic transcutaneous electrical spinal cord stimulation, using a wide range of natural walking speeds, can be applied to control kinematic movement parameters.

     

Interaction between descending input and thoracic reflexes for joint coordination in cockroach: I. Descending influence on thoracic sensory reflexes

Tethered cockroaches turn from unilateral antennal contact using asymmetrical movements of mesothoracic (T2) legs (Mu and Ritzmann in J Comp Physiol A 191:1037–1054, 2005). During the turn, the leg on the inside of the turn (the inside T2 leg) has distinctly different motor patterns from those in straight walking. One possible neural mechanism for the transformation from walking to inside leg turning could be that the descending commands alter a few critical reflexes that start a cascade of physical changes in leg movement or posture, leading to further alterations. This hypothesis has two implications: first, the descending activities must be able to influence thoracic reflexes. Second, one should be able to initiate the turning motor pattern without descending signals by mimicking a point farther down in the reflex cascade. We addressed the first implication in this paper by experiments on chordotonal organ reflexes. The activity of depressor muscle (Ds) and slow extensor tibia muscle (SETi) was excited and inhibited by stretching and relaxing the femoral chordotonal organ. However, the Ds responses were altered after eliminating the descending activity, while the SETi responses remain similar. The inhibition to Ds activity by stretching the coxal chordotonal organ was also altered after eliminating the descending activity.     

Stick insects walking along inclined surfaces

In the experiments stick insects walk on an inclined substratesuch that the legs of one side of the body point uphill andthe legs of the other side point downhill. In this situationthe vertical axis of the body is rotated against the inclinationof the substrate as if to compensate for the effect of substrateinclination. A very small effect has been found when the experimentwas performed with animals standing on a tilted platform whichshows that the effect depends on the behavioral context. When,however, animals first walked along the inclined surface andthen, before measurement, stopped walking spontaneously, a rotationof the body has been observed similar to that in walking animals.In a second experiment it was tested whether the observed bodyrotation is caused by the change of direction of gravity vectoror by the fact that on an inclined surface gravity necessarilyhas a component pulling the body sideways. Experiments withanimals standing on horizontal ground and additional weightsapplied pulling the body to the side showed similar body rotationssupporting the latter idea. In a simulation study it could beshown that the combined activity of proportional feedback controllersin the leg joints is sufficient to explain the observed behavior.This is however only possible if the gain factors of coxa-trochanterjoint controller and of femur-tibia joint controller show aratio in the order of 1 : 0.05 to 1 : 1.8. In order to describethe behavior of animals standing on a tilted platform, a ratioof 1 : 1.7 is necessary. In walking animals, this body rotationrequires to change the trajectories of stance and swing movements.The latter have been studied in more detail. During swing, thefemur-tibia joint is more extended in the uphill legs. Conversely,the coxa-trochanter joint appears to be more elevated in thedownhill legs which compensates the smaller lift in the femur-tibiajoint. The results are discussed in the context of differenthypotheses.     

System identification of muscle–joint interactions of the cat hind limb during locomotion

Neurophysiological experiments in walking cats have shown that a number of neural control mechanisms are involved in regulating the movements of the hind legs during locomotion. It is experimentally hard to isolate individual mechanisms without disrupting the natural walking pattern and we therefore introduce a different approach where we use a model to identify what control is necessary to maintain stability in the musculo-skeletal system. We developed a computer simulation model of the cat hind legs in which the movements of each leg are produced by eight limb muscles whose activations follow a centrally generated pattern with no proprioceptive feedback. All linear transfer functions, from each muscle activation to each joint angle, were identified using the response of the joint angle to an impulse in the muscle activation at 65 postures of the leg covering the entire step cycle. We analyzed the sensitivity and stability of each muscle action on the joint angles by studying the gain and pole plots of these transfer functions. We found that the actions of most of the hindlimb muscles display inherent stability during stepping, even without the involvement of any proprioceptive feedback mechanisms, and that those musculo-skeletal systems are acting in a critically damped manner, enabling them to react quickly without unnecessary oscillations. We also found that during the late swing, the activity of the posterior biceps/semitendinosus (PB/ST) muscles causes the joints to be unstable. In addition, vastus lateralis (VL), tibialis anterior (TA) and sartorius (SAT) muscle-joint systems were found to be unstable during the late stance phase, and we conclude that those muscles require neuronal feedback to maintain stable stepping, especially during late swing and late stance phases. Moreover, we could see a clear distinction in the pole distribution (along the step cycle) for the systems related to the ankle joint from that of the other two joints, hip or knee. A similar pattern, i.e., a pattern in which the poles were scattered over the s-plane with no clear clustering according to the phase of the leg position, could be seen in the systems related to soleus (SOL) and TA muscles which would indicate that these muscles depend on neural control mechanisms, which may involve supraspinal structures, over the whole step cycle.