Leg kinematics and muscle activity during treadmill running in the cockroach, Blaberus discoidalis : I. Slow running

We have combined high-speed video motion analysis of leg movements with electromyogram (EMG) recordings from leg muscles in cockroaches running on a treadmill. The mesothoracic (T2) and metathoracic (T3) legs have different kinematics. While in each leg the coxa-femur (CF) joint moves in unison with the femur-tibia (FT) joint, the relative joint excursions differ between T2 and T3 legs. In T3 legs, the two joints move through approximately the same excursion. In T2 legs, the FT joint moves through a narrower range of angles than the CF joint. In spite of these differences in motion, no differences between the T2 and T3 legs were seen in timing or qualitative patterns of depressor coxa and extensor tibia activity. The average firing frequencies of slow depressor coxa (Ds) and slow extensor tibia (SETi) motor neurons are directly proportional to the average angular velocity of their joints during stance. The average Ds and SETi firing frequency appears to be modulated on a cycle-by-cycle basis to control running speed and orientation. In contrast, while the frequency variations within Ds and SETi bursts were consistent across cycles, the variations within each burst did not parallel variations in the velocity of the relevant joints. Accepted: 24 May 1997     

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.     

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     

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.     

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.     

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.     

Control of climbing behavior in the cockroach, Blaberus discoidalis. II. Motor activities associated with joint movement

Deathhead cockroaches employ characteristic postural strategies for surmounting barriers. These include rotation of middle legs to re-direct leg extension and drive the animal upward. However, during climbing the excursions of the joints that play major roles in leg extension are not significantly altered from those seen during running movements. To determine if the motor activity associated with these actions is also unchanged, we examined the electromyogram activity produced by the slow trochanteral extensor and slow tibial extensor motor neurons as deathhead cockroaches climbed over obstacles of two different heights. As they climbed, activity in the slow trochanteral extensor produced a lower extension velocity of the coxal-trochanteral joint than the same frequency of slow trochanteral extensor activity produces during horizontal running. Moreover, the pattern of activity within specific leg cycles was altered. During running, the slow trochanteral extensor generates a high-frequency burst prior to foot set-down. This activity declines through the remainder of the stance phase. During climbing, motor neuron frequency no longer decreased after foot set-down, suggesting that reflex adjustments were made. This conclusion was further supported by the observation that front leg amputees generated even stronger slow trochanteral extensor activity in the middle leg during climbing movements.     

Vibration signals from the FT joint can induce phase transitions in both directions in motoneuron pools of the stick insect walking system

The influence of vibratory signals from the femoral chordotonal organ fCO on the activities of muscles and motoneurons in the three main leg joints of the stick insect leg, i.e., the thoraco-coxal (TC) joint, the coxa-trochanteral (CT) joint, and the femur-tibia (FT) joint, was investigated when the animal was in the active behavioral state. Vibration stimuli induced a switch in motor activity (phase transition), for example, in the FT joint motor activity switched from flexor tibiae to extensor tibiae or vice versa. Similarly, fCO vibration induced phase transitions in both directions between the motoneuron pools of the TC joint and the CT joint. There was no correlation between the directions of phase transition in different joints. Vibration stimuli presented during simultaneous fCO elongation terminated the reflex reversal motor pattern in the FT joint prematurely by activating extensor and inactivating flexor tibiae motoneurons. In legs with freely moving tibia, fCO vibration promoted phase transitions in tibial movement. Furthermore, ground vibration promoted stance-swing transitions as long as the leg was not close to its anterior extreme position during stepping. Our results provide evidence that, in the active behavioral state of the stick insect, vibration signals can access the rhythm generating or bistable networks of the three main leg joints and can promote phase transitions in motor activity in both directions. The results substantiate earlier findings on the modular structure of the single-leg walking pattern generator and indicate a new mechanism of how sensory influence can contribute to the synchronization of phase transitions in adjacent leg joints independent of the walking direction.     

Motion analysis of leg joints associated with escape turns of the cockroach,Periplaneta americana

Considerable information is now available on the neural organization of the escape system of the American cockroach. To relate these data to the behavior, we need detailed information on the movements made at the principle leg joints that produce the turn. We used motion analysis of high speed video records to acquire such information. Records from both free ranging and tethered animals were analyzed. 1. We analyzed individual joint movements using a tethered preparation. Stimuli from 4 different angles around the animal were used. For all wind angles, the femur-tibia (FT) joint on the mesothoracic leg that is ipsilateral to the wind source extended while the contralateral mesothoracic FT joint flexed. This moved both of these legs laterally toward the wind source. In freely moving animals the FT movements provide forces that turn the animal away from the wind source. 2. The ipsilateral mesothoracic coxa-femur (CF) joint extended for all wind angles. The contralateral mesothoracic CF joint extended in response to most winds from the rear, but switched to flexion in response to wind from the side and front. As a result of these joint movements, rear wind resulted in rearward movements of the contralateral mesothoracic leg, while side and front wind resulted in more forward movements of that leg. 3. The CF and FT joints for both ipsilateral and contralateral metathoracic legs extended to wind from the rear and switched to flexion as the wind was placed at more anterior positions around the animal. In freely moving animals, extension of these joints would push the animal forward. Flexion would pull the animal backward. 4. Several of the joints showed correlations between rate of movement and initial joint angle. That is, joints that were already flexed at the onset of stimulation tended to move at a faster rate to a final position than joints that started at a more extended position. 5. Metathoracic FT and CF joints showed a high degree of positive correlation during the escape movements. Indeed, many curves showing movement of metathoracic FT and CF joints with time were virtually identical.     

Leg coordination during turning on an extremely narrow substrate in a bug, Mesocerus marginatus (Heteroptera, Coreidae)

The turning movement of a bug, Mesocerus marginatus, is observed when it walks upside-down below a horizontal beam and, at the end of the beam, performs a sharp turn by 180 degrees . The turn at the end of the beam is accomplished in three to five steps, without strong temporal coordination among legs. During the stance, leg endpoints (tarsi) run through rounded trajectories, rotating to the same side in all legs. During certain phases of the turn, a leg is strongly depressed and the tarsus crosses the midline. Swing movements rotate to the same side as do leg endpoints in stance, in strong contrast to the typical swing movements found in turns or straight walk on a flat surface. Terminal location is found after the search through a trajectory that first moves away from the body and then loops back to find substrate. When a leg during stance has crossed the midline, in the following swing movement the leg may move even stronger on the contralateral side, i.e. is stronger depressed, in contrast to swing movements in normal walking, where the leg is elevated. These results suggest that the animals apply a different control strategy compared to walking and turning on a flat surface.     

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.     

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.     

Take-off and the 'tarsal reflex' in Aphis fabae

ABSTRACT. In the transition from walking to flight in free and tethered aphids, forward progression was more or less abruptly checked and the walking pattern of leg movements gave way to a stationary, treading phase. This was followed by leg extension and wing-spreading, kicking of the mesothoracic legs, wing-beating and final lift-off. Removal of the wings, but not of the middle legs, inhibited this pre-take-off behaviour. Jumping appeared to play no part in takeoff, nor did loss of tarsal contact stimulate flight in tethered aphids but resulted only in wing-raising. However, restoration of tarsal contact often resulted in immediate take-off, as well as stimulating post-flight wing-folding, Wing-beating, but not wing-raising, was apparently inhibited during walking.     

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.     

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.     

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.     

The structure and function of serially homologous leg motor neurons in the locust. I. Anatomy

Twenty-one prothoracic and 17 mesothoracic motor neurons innervating leg muscles have been identified physiologically and subsequently injected with dye from a microelectrode. A tract containing the primary neurites of motor neurons innervating the retractor unquis, levator and depressor tarsus, flexor tibiae, and reductor femora is described. All motor neurons studied have regions in which their dendritic branches overlap with those of other leg motor neurons. Identified, serially homologous motor neurons in the three thoracic ganglia were found to have: (1) cell bodies at similar locations and morphologically similar primary neurites (e.g., flexor tibiae motor neurons), (2) cell bodies at different locations in each ganglion and morphologically different primary neurites in each ganglion (e.g., fast retractor unguis motor neurons), or (3) cell bodies at similar locations and morphologically similar primary neurites but with a functional switch in one ganglion relative to the function of the neurons in the other two ganglia. As an example of the latter, the morphology of the metathoracic slow extensor tibiae (SETi) motor neurons was similar to that of pro- and mesothoracic fast extensor tibiae (FETi) motor neurons. Similarly the metathoracic FETi bears a striking resemblance to the pro- and the mesothoracic SETi. It is proposed that in the metathoracic ganglion the two extensor tibiae motor neurons have switched functions while retaining similar morphologies relative to the structure and function of their pro- and mesothoracic serial homologues.     

Functional recovery following manipulation of muscles and sense organs in the stick insect leg

We studied functional recovery of leg posture and walking behaviour in the femur-tibia joint control system of stick insects. Leg extensions in resting animals and during walking are produced by different parts of a single extensor muscle. (a) Ablation of the muscle part responsible for fast movements prevented leg extension during the swing phase. Resting posture remained unaffected. Within a few post-operative days, extension movements recovered, provided that sensory feedback was available. Extension movements were now driven by the muscle part which in intact animals controls the resting posture only. (b) Selective ablation of this (slow) muscle part affected the resting posture, while walking was unaffected. The resting posture partly recovered during subsequent days. To test the range of functional recovery and underlying mechanisms, we additionally transected muscle motor innervation, or we inverted or ablated sensory feedback. We found that recovery was based on both muscular and neuronal mechanisms. The latter required appropriate sensory feedback for the process of recovery, but not for the maintenance of the recovered state. Our results thus indicate the existence of a sensory template that guides recovery. Recovery was limited to a behavioural range that occurs naturally in intact animals, though in different behavioural contexts.     

Proprioceptive regulation of locomotion

Recent investigations of proprioreceptors in the walking systems of cats, insects and crustaceans have identified reflex pathways that regulate the timing of the transition from stance to swing, and control the magnitude of ongoing motoneuronal activity. An important finding in the cat is that during locomotor activity, the influence of feedback from the Golgi tendon organs in extensor muscles onto extensor motoneurons is reversed from inhibition to excitation. The excitatory action of tendon organs during stance ensures that stance is maintained while extensor muscles are loaded, and may regulate the magnitude of extensor activity according to the load carried by the leg. Afferents from primary and secondary spindles in extensor and flexor muscles have also been found to influence the timing of the locomotor rhythm in a functionally relevant manner. Recent studies indicate that reflex reversals and the regulation of timing by multiple proprioceptive systems are also features of walking systems in arthropods.     

Leg kinematics and muscle activity during treadmill running in the cockroach, Blaberus discoidalis: II. Fast running

We have combined kinematic and electromyogram (EMG) analysis of running Blaberus discoidalis to examine how middle and hind leg kinematics vary with running speed and how the fast depressor coxa (Df) and fast extensor tibia (FETi) motor neurons affect kinematic parameters. In the range 2.5–10 Hz, B. discoidalis increases step frequency by altering the joint velocity and by reducing the time required for the transition from flexion to extension. For both Df and FETi the timing of recruitment coincides with the maximal frequency seen for the respective slow motor neurons. Df is first recruited at the beginning of coxa-femur (CF) extension. FETi is recruited in the latter half of femur-tibia (FT) extension during stance. Single muscle potentials produced by these fast motor neurons do not have pronounced effects on joint angular velocity during running. The transition from CF flexion to extension was abbreviated in those cycles with a Df potential occurring during the transition. One effect of Df activity during running may be to phase shift the beginning of joint extension so that the transition is sharpened. FETi is associated with greater FT extension at higher running speeds and may be necessary to overcome high joint torques at extended FT joint angles. Accepted: 24 May 1997