Trochanteral Depressor Research Articles

Force feedback reinforces muscle synergies in insect legs

The nervous system solves complex biomechanical problems by activating muscles in modular, synergist groups. We have studied how force feedback in substrate grip is integrated with effects of sense organs that monitor support and propulsion in insects. Campaniform sensilla are mechanoreceptors that encode forces as cuticular strains. We tested the hypothesis that integration of force feedback from receptors of different leg segments during grip occurs through activation of specific muscle synergies. We characterized the effects of campaniform sensilla of the feet (tarsi) and proximal segments (trochanter and femur) on activities of leg muscles in stick insects and cockroaches. In both species, mechanical stimulation of tarsal sensilla activated the leg muscle that generates substrate grip (retractor unguis), as well as proximal leg muscles that produce inward pull (tibial flexor) and support/propulsion (trochanteral depressor). Stimulation of campaniform sensilla on proximal leg segments activated the same synergistic group of muscles. In stick insects, the effects of proximal receptors on distal leg muscles changed and were greatly enhanced when animals made active searching movements. In insects, the task-specific reinforcement of muscle synergies can ensure that substrate adhesion is rapidly established after substrate contact to provide a stable point for force generation.

Jumping mechanisms in flatid planthoppers (Hemiptera, Flatidae)

The jumping performance of three species of hemipterans from Australia and Europe belonging to the family Flatidae was analysed from images captured at a rate of 5000 s(-1). The shape of a flatid was dominated by large triangular or wedge-shaped front wings, which, when folded, covered and extended above and behind the body to give a laterally compressed and possibly streamlined appearance. The body lengths of the three species of adults ranged from 7 to 9 mm and their mass from 8 to 19 mg. The propulsive hind legs were 30% longer than the front legs but only 36-54% of the body length. Jumps with the fastest take-off velocities of 2.8-3.2 m s(-1) had acceleration times of 1.4-1.8 ms. During such jumps, adults experienced an acceleration of 174-200 G: . These jumps required an energy expenditure of 76-225 μJ, a power output of 13-60 mW and exerted a force of 9-37 mN. The required power output per mass of jumping muscle in adults ranged from 24,000 to 27,000 W kg(-1) muscle, 100 times greater than the maximum active contractile limit of normal muscle. The free-living nymphs were also proficient jumpers, reaching take-off velocities of 2.2 m s(-1). To achieve such a jumping performance requires a power amplification mechanism. The energy store for such a mechanism was identified as the internal skeleton linking a hind coxa to the articulation of a hind wing. These pleural arches fluoresced bright blue when illuminated with UV light, indicating the presence of the elastic protein resilin. The energy generated by the prolonged contractions of the trochanteral depressor muscles was stored in distortions of these structures, and the rapid elastic recoil of these muscles powered the synchronous propulsive movements of the hind legs.

Jumping mechanisms in lacewings (Neuroptera, Chrysopidae and Hemerobiidae).

Lacewings launch themselves into the air by simultaneous propulsive movements of the middle and hind legs as revealed in video images captured at a rate of 1000 s(-1). These movements were powered largely by thoracic trochanteral depressor muscles but did not start from a particular preset position of these legs. Ridges on the lateral sides of the meso- and metathorax fluoresced bright blue when illuminated with ultraviolet light, suggesting the presence of the elastic protein resilin. The middle and hind legs were longer than the front legs but their femora and tibiae were narrow tubes of similar diameter. Jumps were of two types. First, those in which the body was oriented almost parallel to the ground (-7±8 deg in green lacewings, 13.7±7 deg in brown lacewings) at take-off and remained stable once animals were airborne. The wings did not move until 5 ms after take-off when flapping flight ensued. Second, were jumps in which the head pointed downwards at take-off (green lacewings, -37±3 deg; brown lacewings, -35±4 deg) and the body rotated in the pitch plane once airborne without the wings opening. The larger green lacewings (mass 9 mg, body length 10.3 mm) took 15 ms and the smaller brown lacewings (3.6 mg and 5.3 mm) 9 ms to accelerate the body to mean take-off velocities of 0.6 and 0.5 m s(-1). During their fastest jumps green and brown lacewings experienced accelerations of 5.5 or 6.3 G: , respectively. They required an energy expenditure of 5.6 or 0.7 μJ, a power output of 0.3 or 0.1 mW and exerted a force of 0.6 or 0.2 mN. The required power was well within the maximum active contractile limit of normal muscle, so that jumping could be produced by direct muscle contractions without a power amplification mechanism or an energy store.

Force encoding in stick insect legs delineates a reference frame for motor control

The regulation of forces is integral to motor control. However, it is unclear how information from sense organs that detect forces at individual muscles or joints is incorporated into a frame of reference for motor control. Campaniform sensilla are receptors that monitor forces by cuticular strains. We studied how loads and muscle forces are encoded by trochanteral campaniform sensilla in stick insects. Forces were applied to the middle leg to emulate loading and/or muscle contractions. Selective sensory ablations limited activities recorded in the main leg nerve to specific receptor groups. The trochanteral campaniform sensilla consist of four discrete groups. We found that the dorsal groups (Groups 3 and 4) encoded force increases and decreases in the plane of movement of the coxo-trochanteral joint. Group 3 receptors discharged to increases in dorsal loading and decreases in ventral load. Group 4 showed the reverse directional sensitivities. Vigorous, directional responses also occurred to contractions of the trochanteral depressor muscle and to forces applied at the muscle insertion. All sensory discharges encoded the amplitude and rate of loading or muscle force. Stimulation of the receptors produced reflex effects in the depressor motoneurons that could reverse in sign during active movements. These data, in conjunction with findings of previous studies, support a model in which the trochanteral receptors function as an array that can detect forces in all directions relative to the intrinsic plane of leg movement. The array could provide requisite information about forces and simplify the control and adaptation of posture and walking.

Encoding of force increases and decreases by tibial campaniform sensilla in the stick insect, Carausius morosus

Detection of force increases and decreases is important in motor control. Experiments were performed to characterize the structure and responses of tibial campaniform sensilla, receptors that encode forces through cuticular strains, in the middle leg of the stick insect (Carausius morosus). The sensilla consist of distinct subgroups. Group 6A sensilla are located 0.3mm distal to the femoro-tibial joint and have oval shaped cuticular caps. Group 6B receptors are 1mm distal to the joint and have round caps. All sensilla show directional, phasico-tonic responses to forces applied to the tibia in the plane of joint movement. Group 6B sensilla respond to force increases in the direction of joint extension while Group 6A receptors discharge when those forces decrease. Forces applied in the direction of joint flexion produce the reverse pattern of sensory discharge. All receptors accurately encode the rate of change of force increments and decrements. Contractions of tibial muscles also produce selective, directional sensory discharges. The subgroups differ in their reflex effects: Group 6B receptors excite and Group 6A sensilla inhibit tibial extensor and trochanteral depressor motoneurons. The tibial campaniform sensilla can, therefore, encode force increases or decreases and aid in adapting motor outputs to changes in load.

Actions of motor neurons and leg muscles in jumping by planthopper insects (hemiptera, issidae)

To understand the catapult mechanism that propels jumping in a planthopper insect, the innervation and action of key muscles were analyzed. The large trochanteral depressor muscle, M133b,c, is innervated by two motor neurons and by two dorsal unpaired median (DUM) neurons, all with axons in N3C. A smaller depressor muscle, M133a, is innervated by two neurons, one with a large-diameter cell body, a large, blind-ending dendrite, and a giant ovoid, axon measuring 50 microm by 30 microm in nerve N5A. The trochanteral levator muscles (M132) and (M131) are innervated by N4 and N3B, respectively. The actions of these muscles in a restrained jump were divisible into a three-phase pattern. First, both hind legs were moved into a cocked position by high-frequency bursts of spikes in the levator muscles lasting about 0.5 seconds. Second, and once both legs were cocked, M133b,c received a long continuous sequence of motor spikes, but the two levators spiked only sporadically. The spikes in the two motor neurons to M133b,c on one side were closely coupled to each other and to the spikes on the other side. If one hind leg was cocked then the spikes only occurred in motor neurons to that side. The final phase was the jump movement itself, which occurred when the depressor spikes ceased and which lasted 1 ms. Muscles 133b,c activated synchronously on both sides, are responsible for generating the power, and M133a and its giant neuron may play a role in triggering the release of a jump.

Energy storage and synchronisation of hind leg movements during jumping in planthopper insects (Hemiptera, Issidae)

The hind legs of Issus (Hemiptera, Issidae) move in the same plane underneath the body, an arrangement that means they must also move synchronously to power jumping. Moreover, they move so quickly that energy must be stored before a jump and then released suddenly. High speed imaging and analysis of the mechanics of the proximal joints of the hind legs show that mechanical mechanisms ensure both synchrony of movements and energy storage. The hind trochantera move first in jumping and are synchronised to within 30 micros. Synchrony is achieved by mechanical interactions between small protrusions from each trochantera which fluoresce bright blue under specific wavelengths of ultra-violet light and which touch at the midline when the legs are cocked before a jump. In dead Issus, a depression force applied to a cocked hind leg, or to the tendon of its trochanteral depressor muscle causes a simultaneous depression of both hind legs. The protrusion of the hind leg that moves first nudges the other hind leg so that both move synchronously. Contractions of the trochanteral depressor muscles that precede a jump bend the metathoracic pleural arches of the internal skeleton. Large areas of these bow-shaped structures fluoresce bright blue in ultraviolet light, and the intensity of this fluorescence depends on the pH of the bathing saline. These are key signatures of the rubber-like protein resilin. The remainder of a pleural arch consists of stiff cuticle. Bending these composite structures stores energy and their recoil powers jumping.

Jumping strategies and performance in shore bugs (Hemiptera, Heteroptera,Saldidae)

The jumping movements of the hemipteran shore bug (Saldula saltatoria, sub-order Heteroptera, family Saldidae) were analysed from sequences of images captured at 5000 frames s(-1). Adult Saldula weigh approximately 2.1 mg and are approximately 3.5 mm long. The hind legs that propel jumping are 180% longer than the front legs and 90% of body length, but non-jumping species in the same family have longer hind legs relative to the lengths of their bodies. Jumps were powered by large trochanteral depressor muscles in the thorax in two different strategies. In the first (used in 24% of jumps analysed), a jump was propelled by simultaneous extension of the two hind legs powered by rapid depression movements about the coxo-trochanteral joints, while both pairs of wings remained closed. In the second strategy (74% of jumps), the wings were opened before the hind legs began to move. At take-off, the position of the wings was variable and could be 8-21 ms into either elevation or depression. When the hind legs alone propelled a jump, the body was accelerated in 3.97+/-0.111 ms at a take-off angle of 52+/-6.5 degrees to a take-off velocity of 1.27+/-0.119 m s(-1); when the wings also moved, the body was accelerated in 3.86+/-0.055 ms at a take-off angle of 58+/-1.7 degrees to a take-off velocity of 1.29+/-0.032 m s(-1). These values are not different in the two jumping strategies. In its best jumps the take-off velocity reached 1.8 m s(-1) so that Saldula experienced an average acceleration of 529 m s(-2), equivalent to almost 54 g, expended 3.4 microJ of energy, while exerting a force of 1.1 m N. The power requirements for jumping indicate that a catapult mechanism must be used in which the trochanteral depressor muscles contract and store energy in advance of a jump. These jumps should propel it to a height of 105 mm or 30 times its body length and distances of 320 mm. The two jumping strategies achieve the same jumping performance.

Resilin and chitinous cuticle form a composite structure for energy storage in jumping by froghopper insects

BackgroundMany insects jump by storing and releasing energy in elastic structures within their bodies. This allows them to release large amounts of energy in a very short time to jump at very high speeds. The fastest of the insect jumpers, the froghopper, uses a catapult-like elastic mechanism to achieve their jumping prowess in which energy, generated by the slow contraction of muscles, is released suddenly to power rapid and synchronous movements of the hind legs. How is this energy stored?ResultsThe hind coxae of the froghopper are linked to the hinges of the ipsilateral hind wings by pleural arches, complex bow-shaped internal skeletal structures. They are built of chitinous cuticle and the rubber-like protein, resilin, which fluoresces bright blue when illuminated with ultra-violet light. The ventral and posterior end of this fluorescent region forms the thoracic part of the pivot with a hind coxa. No other structures in the thorax or hind legs show this blue fluorescence and it is not found in larvae which do not jump. Stimulating one trochanteral depressor muscle in a pattern that simulates its normal action, results in a distortion and forward movement of the posterior part of a pleural arch by 40 μm, but in natural jumping, the movement is at least 100 μm.ConclusionCalculations showed that the resilin itself could only store 1% to 2% of the energy required for jumping. The stiffer cuticular parts of the pleural arches could, however, easily meet all the energy storage needs. The composite structure therefore, combines the stiffness of the chitinous cuticle with the elasticity of resilin. Muscle contractions bend the chitinous cuticle with little deformation and therefore, store the energy needed for jumping, while the resilin rapidly returns its stored energy and thus restores the body to its original shape after a jump and allows repeated jumping.

Neurons controlling jumping in froghopper insects

The neurons innervating muscles that deliver the enormous power enabling froghopper insects to excel at jumping were revealed by backfilling the nerves from those muscles. The huge trochanteral depressor muscle (M133) of a hind leg consists of four parts. The two largest parts (M133b,c) occupy most of the metathorax and are innervated by the same two motor neurons that have small, laterally placed somata in the metathoracic ganglion and axons in nerve N3C(2). They are also supplied by three dorsal unpaired median (DUM) neurons with the largest diameter somata in the central nervous system. A small metathoracic part of the muscle (M133d) is supplied by two motor neurons with lateral somata and by common inhibitory motor neuron CI(1), all with axons in nerve N3C(3) The motor neuron with the larger soma has a thick primary neurite that projects across the midline of the ganglion so that its branches overlap those of its symmetrical counterpart,innervating the same muscle of the other hind leg. The fourth coxal part of the muscle (M133a) is innervated by two motor neurons (one with a ventral and the other with a dorsal and lateral soma), by CI(1), and by a DUM neuron with a small soma. All have axons in nerve N5A. The two trochanteral levator muscles of a hind leg are contained within the coxa and are separately innervated by nerves N3B and N4, respectively. The properties of the different motor neurons are discussed in the context of the neural patterns that generate jumping.

Anatomy of the hind legs and actions of their muscles during jumping in leafhopper insects

The rapid and simultaneous depression of the trochantera about the coxae of both hind legs of leafhoppers are the key joint movements powering a jump. The present study analyses the structure of these joints and the actions of the muscles that move them. The hind coxae are huge and are linked to each other at the midline by a protrusion from one coxa that inserts in a socket of the other and acts like a press-stud (popper) fastener. This asymmetry is not reflected in any left- or right-handed preference either within one species or between species. The movements of the joints in a jump are monitored by a number of possible proprioceptors that should be activated when a hind leg is fully levated in preparation for a jump: a hair row and two hair plates on the coxa, a hair plate on a trochanteral pivot with a coxa, and femoral spines at the femoro-tibial joint. The depressor and levator muscles that move the trochanter are of similar size and together occupy the greater part of the metathorax. Their lever arms are similar when the leg is fully levated, but the lever arm of the depressor increases with initial depression of the coxo-trochanteral joint while that of the levator declines. A jump is preceded by activity in the trochanteral depressor and levator muscles, which results in a forward movement of the coxa and metathorax with the trochanter fully levated. This period of co-contraction could result in storage of energy in skeletal structures in the thorax. Just before the rapid depression of the trochanter in the jump movement the frequency of depressor spikes increases while that in the levator declines, releasing any force stored by the preceding muscle contractions. These bursts of depressor spikes occur at the same time in the left and right muscles but none of the individual motor spikes appeared to be synchronous on the two sides.

Morphology and action of the hind leg joints controlling jumping in froghopper insects

The morphology and movements of key joints of the hind legs that generate the rapid jumping of froghoppers were analysed. The movements of an individual hind leg during a jump occur in three phases. First, the trochanter is slowly levated about the coxa so that the femur moves anteriorly and engages with a lateral protrusion on the coxa. Second, both hind legs are held in this fully levated (cocked) position without moving for a few seconds. Third, both hind legs depress and extend completely in less than 1 ms. The critical, power-generating movement underlying a jump is the rapid and simultaneous depression of the trochantera about the coxae. The lever arm of the hind trochanteral depressor muscle is smallest at the cocked position, but does not appear to go over the centre of the pivot. It then increases to a maximum after some 80 degrees of depression movement. By contrast, the lever arm of the trochanteral levator tendon is similar over the range of joint movements and is exceeded by that of the depressor only after 40 degrees of depression. Three prominent arrays of hairs on the trochantin, coxa and trochanter are appropriately positioned to act as proprioceptors signalling key movements in jumping. In the fully levated position, a protrusion on the dorsal, proximal surface of a hind femur engages with a protrusion from the ventral and lateral part of a coxa. These structures are not present on the front and middle legs. Both protrusions are covered with a dense array of small projections (microtrichia) that both increase the surface area and may interlock with each other. To depress rapidly in a jump these protrusions must disengage. If the hind leg of a dead froghopper is forcibly levated, it will lock in its cocked position, from which it can depress rapidly by movement of the coxo-trochanteral joint and disengagement of the femoral and coxal protrusions. A prominent click sound occurs at the start of a jump that results either from the initial movements of the coxo-trochanteral joint, or from the disengagement of the microtrichia on the coxa and femur. Larval Philaenus, which do not jump, lack a femoral protrusion and have no microtrichia in equivalent positions on either the coxa or femur.

Neural Control and Coordination of Jumping in Froghopper Insects

The thrust for jumping in froghopper insects is produced by a rapid, synchronous depression of both hind legs generated by huge, multipartite trochanteral depressor muscles in the thorax and smaller levator muscles in the coxae. A three-phase motor pattern activates these muscles in jumping. First, a levation phase lasts a few hundred milliseconds, in which a burst of spikes in the trochanteral levator motor neurons moves the hind legs into their fully cocked position and thus engages a mechanical lock between a coxa and a femur. Second, a cocked phase lasts a few seconds, in which a trochanteral depressor motor neuron spikes continuously at a frequency gradually rising to 50 Hz, although the hind legs remain stationary. Levator motor spikes are sporadic. Third, the jump movement lasts <1 ms, in which the spikes in the depressors stop abruptly and the legs rapidly depress. This pattern may vary in the speed of the initial levation and in the duration of the cocked phase. Recordings from the depressor muscles on both sides showed remarkable synchrony of their motor spikes. In one 4.9-long cocked phase all 174 spikes were synchronous and in another 27 s period of continuous spiking all but one of 1,176 spikes were synchronous. When a single hind leg moves rapidly, these depressor spikes are nevertheless independent of those of the other leg. These features of the motor pattern and the coupling between motor neurons to the two hind legs ensure powerful movements to propel rapid jumping.

Central Generation of Grooming Motor Patterns and Interlimb Coordination in Locusts

Coordinated bursts of leg motoneuron activity were evoked in locusts with deefferented legs by tactile stimulation of sites that evoke grooming behavior. This suggests that insect thoracic ganglia contain central pattern generators for directed leg movements. Motoneuron recordings were made from metathoracic and mesothoracic nerves, after eliminating all leg motor innervation, as well as all input from the brain, subesophageal ganglion, and prothoracic ganglion. Strong, brief trochanteral levator motoneuron bursts occurred, together with silence of the slow and fast trochanteral depressor motoneurons and activation of the common inhibitor motoneuron. The metathoracic slow tibial extensor motoneuron was active in a pattern distinct from its activity during walking or during rhythms evoked by the muscarinic agonist pilocarpine. Preparations in which the metathoracic ganglion was isolated from all other ganglia could still produce fictive motor patterns in response to tactile stimulation of metathoracic locations. Bursts of trochanteral levator and depressor motoneurons were clearly coordinated between the left and right metathoracic hemiganglia and also between the mesothoracic and the ipsilateral metathoracic ganglia. These data provide clear evidence for centrally generated interlimb coordination in an insect.

The jumping mechanism of Xenopsylla cheopis. III. Execution of the jump and activity.

The flea's hind legs are the chief source of jumping power, but in species which execute large jumps, take-off is accelerated by elastic energy released from a resilin pad (homologous with the wing hinge ligaments of flying insects) situated in the pleural arch. A central click mechanism, operated by a rapid twitch of the trochanteral depressor (the starter muscle), synchronizes the separate sources of energy which power the jump. Ciné photos confirm the morphological evidence that the flea takes off from the trochanters, not the tarsi. The loss of wings, associated with lateral compression of the body and the shortening of the pleural ridge (which thus lowers the position of the pleural arch) together with modifications of the direct and indirect flight muscles, are some of the main morphological features associated with the change from a flying to a saltatorial mode of progression. The flea's take-off basically resembles that of other Panorpoid insects (Diptera, Mecoptera, etc.). The release of elastic energy from the pleural arch is a system by which the force used to move the wings of flying insects is rapidly fed back into the legs and adds power to the jump.

The jumping mechanism of Xenopsylla cheopis. II. The fine structure of the jumping muscle.

The ultrastructure of the trochanteral depressor muscle of the oriental rat flea is described. It is shown to be similar to that of the tubular leg muscles of other insects except in the volume and arrangement of the sarcoplasmic reticulum. The sarcoplasmic reticulum occupies approximately 18% of the volume of the muscle fibres. It is in three configurations:a regular array of parallel tubules opposite the A-band, a collar of sacculi involved in the formation of the dyads at the edge of the A-band and a loosely woven arrangement of tubules around the I-band. This tripartite arrangement of the sarcoplasmic reticulum and its large surface area is discussed in relation to the action of the muscle as the main propulsive muscle in the jump of the flea.

Non-fibrillar muscles and the start and cessation of flight in the milkweed bug,Oncopeltus

1. The behavioural sequence at the start of flight inOncopeltus has been analysed by high speed photography (Fig. 1). The flight muscles (in particular the non-fibrillar ones) responsible for this behaviour have been identified by electrical recordings, ablation experiments and anatomical evidence. 2. The release of the wing base by the prothoracic lobe is assigned to the prothoracic dorsoventralis and mesosterni primus muscles on anatomical evidence. 3. The wing opening, consisting of unlocking and unfolding of the fore wings, is performed by a high frequency discharge of a motor neuron of the tergal promoter, remotor and tergotrochanteral muscles (Fig. 5). Non-flight wing opening is also similarly achieved (Fig. 6). 4. It is argued that the action of the leg muscles additionally triggers the oscillatory contractions of the myogenic motor by stretching the neurally activated dorsal longitudinal muscle. Thus the first half stroke in flight is a downstroke which serves to link the fore and hind wings. 5. At the start of flight the click mechanism in the wing articulation is put into operation by contraction of the tonic pleurofurcal muscle (Fig. 8) which adjusts the lateral stiffness of the thoracic box. 6. The take-off jump occurs after flight has started and is executed by a complex of trochanteral depressor muscles of the meso- and metathoracic legs (Fig. 9). 7. At the end of flight the wings are flexed and locked by the firing of a motor neuron in the episterno-alaris muscle (Fig. 10).

Developmental Interactions in the Development of the Imaginal Muscles of Drosophila

ABSTRACT The thorax of Drosophila contains two main sets of muscles, the dorsal flight-muscles and a lateral set. Among the latter are the trochanteral depressors of the legs, of which those associated with the second legs are the largest. The development of all these muscles during the pupal period is described and an account is given of the effects of the contraction of the tendons of the longitudinal muscles in producing the curvature of the mesothorax and the formation of the post-notum. The dorsal flight-muscles develop from an interaction between (a) three pairs of larval muscles; (b) mesoderm cells derived from the mesothoracic imaginal buds; (c) cells which migrate from the developing trochanteral depressors of the second leg. It is the latter cells which are responsible for splitting the three larval muscles of each side into six. The fibrillar muscles of the lateral set have a similar origin. The trochanteral depressors are tubular, not fibrillar, in structure. They are formed from mesoderm cells of the leg imaginal buds. If the imaginal bud of a first or third leg is removed from the late larva, not only the leg but also the corresponding trochanteral depressor is missing from the adult. If a second leg bud is removed, the dorsal flight-muscles and the lateral fibrillar muscles on that side also fail to develop. In extreme bithorax phenotypes, in which the metathoracic bud has formed a structure externally resembling a mesothorax, this region does not contain a second set of flight-muscles, although there are sometimes small badly differentiated representations of them. The secondary scutellum is not provided with a post-notum. If the normal mesothoracic bud of one side is extirpated from a larva which is developing the bithorax phenotype, the transformed metathoracic bud may shift forward and fuse with the mesothoracic bud of the opposite side. In some such cases the metathoracic mesoderm, in association with cells from the second trochanteral depressor, has developed into flight-muscles. It is concluded that the migrating cells of the second trochanteral depressor provide a stimulus which is essential for the differentiation of the flight-muscles.