Local innervation patterns of the metathoracic flexor and extensor tibiae motor neurons in the cricket Gryllus bimaculatus

To elucidate neural mechanisms underlying walking and jumping in insects, motor neurons supplying femoral muscles have been identified mainly in locusts and katydids, but not in crickets. In this study, the motor innervation patterns of the metathoracic flexor and extensor tibiae muscles in the cricket, Gryllus bimaculatus were investigated by differential back-fills and nerve recordings. Whereas the extensor tibiae muscle has an innervation pattern similar to that of other orthopterans, the flexor has an innervation unique to this species. The main body of the flexor muscle is divided into the proximal, middle and distal regions, which receive morphologically unique terminations from almost non-overlapping sets of motor neurons. The proximal region is innervated by about 12 moderate-sized excitatory motor neurons and two inhibitory neurons while the middle and distal regions are innervated by three and four large excitatory motor neurons, respectively. The most-distally located accessory flexor muscle, inserting on a common flexor apodeme with the main muscle, is innervated by at least four small excitatory (slow-type) and two common inhibitory motor neurons. The two excitatory and two inhibitory motor neurons that innervate the accessory flexor muscle also innervate the proximal bundles of the main flexor muscle. This suggests that the most proximal and distal parts of the flexor muscle participate synergistically in fine motor control while the rest participates in powerful drive of tibial flexion movement.     

Sensorimotor pathways processing vibratory signals from the femoral chordotonal organ of the stick insect

The femoral chordotonal organ of stick insects senses position and velocity of movements in the femur-tibia joint, as well as tibial vibration. While sensory information about large-scale tibial movements is processed by a well-known neuronal network and elicits resistance reflexes in extensor and flexor tibiae motoneurons, it is not yet known how sensory information about vibration of the tibia is processed. We investigated the transmission of vibration stimuli to tibial extensor motoneurons and their premotor interneurons. Vibration stimuli applied to the femoral chordotonal organ evoked responses in tibial extensor and flexor muscles. During ongoing vibration this response adapted rapidly. This adaptation had no effect on the motoneuronal response to large-scale tibial movements. Recording from premotor interneurons revealed that vibratory signals were processed in part by the same interneuronal pathways as (large-scale) velocity and position information. While only certain parts of the interneuronal reflex pathways showed little or no response during vibration stimuli, most neurons responded to both position or velocity stimuli and vibration at the femoral chordotonal organ. We conclude that sensory information about vibration of the tibia shares part of the interneuronal pathways that transmit sensory information about large-scale tibial movements to the motoneurons. Accepted: 25 April 1999     

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

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

Motor patterns during kicking movements in the locust

Locusts (Schistocerca gregaria) use a distinctive motor pattern to extend the tibia of a hind leg rapidly in a kick. The necessary force is generated by an almost isometric contraction of the extensor tibiae muscle restrained by the co-contraction of the flexor tibiae (co-contraction phase) and aided by the mechanics of the femoro-tibial joint. The stored energy is delivered suddenly when the flexor muscle is inhibited. This paper analyses the activity of motor neurons to the major hind leg muscles during kicking, and relates it to tibial movements and the resultant forces.During the co-contraction phase flexor tibiae motor neurons are driven by apparently common sources of synaptic inputs to depolarized plateaus at which they spike. The two excitatory extensor motor neurons are also depolarized by similar patterns of synaptic inputs, but with the slow producing more spikes at higher frequencies than the fast. Trochanteral depressors spike at high frequency, the single levator tarsi at low frequency, and common inhibitors 2 and 3 spike sporadically. Trochanteral levators, depressor tarsi, and a retractor unguis motor neuron are hyperpolarized.Before the tibia extends all flexor motor neurons are hyperpolarized simultaneously, two common inhibitors, and the levator trochanter and depressor tarsi motor neurons are depolarized. Later, but still before the tibial movement starts, the extensor tibiae and levator tarsi motor neurons are hyperpolarized. After the movement has started, the extensor motor neurons are hyperpolarized further and the depressor trochanteris motor neurons are also hyperpolarized, indicating a contribution of both central and sensory feedback pathways.Variations in the duration of the co-contraction of almost twenty-fold, and in the number of spikes in the fast extensor tibiae motor neuron from 2–50 produce a spectrum of tibial extensions ranging from slow and weak, to rapid and powerful. Flexibility in the networks producing the motor pattern therefore results in a range of movements suited to the fluctuating requirements of the animal.     

Two antagonistic functions of neural groups of the femoral chordotonal organ underlie thanatosis in the cricket Gryllus bimaculatus DeGeer

The cricket Gryllus bimaculatus displayed freezing (thanatosis) after struggling while the femoro-tibial joints of the walking legs were forcibly restrained. Myographic recording indicated that strong contraction of the flexor tibia muscle “leg flexion response” occurred under this restrained condition. During thanatosis, when the femoro-tibial joint was passively displaced and held for several seconds, it maintained its new position (catalepsy). Only discharge of the slow flexor units was mechanically indispensable for maintaining thanatosis and catalepsy. Differing roles of identified neuron subgroups of the femoral chordotonal organ were elucidated using this behavioral substrate. Ablation of the dorsal group neurons in the ventral scoloparium strengthened the leg flexion response and the normal resistance reflex, while ablation of the ventral group weakened both motor outputs. Ablation of the dorsal scoloparium neurons, or other main sensory nerves caused no detectable deficiency in femoro-tibial joint control. These results imply that both modes of flexor muscle activation promoted by the ventral group neurons are normally held under inhibitory control by the dorsal group. It is hypothesized that this antagonistic function causes immobilization of the femoro-tibial joint in a wide range of angles in thanatosis and catalepsy. Accepted: 12 November 1998     

Leg position learning by an insect: II. Motor strategies underlying learned leg extension

The patterns of myographic activity in the flexor and extensor tibiae muscles of the locust which accompany learned tibial extension were examined. Three distinct motor strategies were identified: (1) repeated flexion-extension movements, each of which resulted in a momentary excursion beyond the required, pre-set joint angle (demand angle) and in sum met the criterion for learning; (2) changes in basic muscle tonus, which resulted in maintained shifts in tibial position without discernible myographic activity; (3) tonic activity in the single slow excitatory motoneuron of the extensor tibiae ( SETi ) which produced maintained tibial extension. These strategies were selectively employed depending on the particular range of joint angle required. These strategies were compared and their effectiveness evaluated using a variety of behavioral criteria. Neuronal mechanisms which might underlie each of these strategies are discussed.     

Assisting components within a resistance reflex of the stick insect, Cuniculina impigra

ABSTRACT. Rapid relaxation (shortening) of the femoral chordotonal organ in Cuniculina impigra Redtenbacher induces a depolarization followed by hyperpolarization of the fast and slow extensor tibiae motor neurons (FETi and SETi). The initial depolarization is caused by acceleration-sensitive units of the chordotonal organ. The reverse sequence of responses is induced in flexor motor neurons. The common inhibitor neuron (CI) is depolarized by both lengthening (stretch) and relaxation of the chordotonal organ.
The initial depolarization of FETi and SETi and the initial hyperpolarization of flexor motor neurons produced by rapid relaxation of the chordotonal organ and the depolarization of CI produced by lengthening of the chordotonal organ all oppose the resistance reflex response. However, these assisting components are weak compared to the resisting ones.     

Proprioceptive feedback in locust kicking and jumping during maturation

Campaniform sensilla monitor the forces generated by the leg muscles during the co-contraction phase of locust (Schistocerca gregaria) kicking and jumping and re-excite the fast extensor (FETi) and flexor tibiae motor neurones, which innervate the leg muscles. Sensory signals from a campaniform sensillum on the proximal tibia were compared in newly moulted locusts, which do not kick and jump, and mature locusts which readily kick and jump. The activity pattern of FETi during co-contraction was mimicked by stimulating the extensor tibiae muscle. Less force was generated and the spike frequency of the sensory neurone from the sensillum was significantly lower in newly moulted compared to mature locusts. Depolarisation of both FETi and flexor motor neurones as a result of sensory feedback was consequently less in newly moulted than in mature locusts. The difference in the depolarisation was greater than the decrease in the afferent spike frequency suggesting that the central connections of the afferents are modulated. The depolarisation could generate spikes in FETi and maintain flexor spikes in mature but not in newly moulted locusts. This indicates that feedback from the anterior campaniform sensillum comprises a significant component of the drive to both FETi and flexor activity during co-contraction in mature animals and that the changes in this feedback contribute to the developmental change in behaviour.Abbreviations aCS anterior campaniform sensillum - ETi extensor tibiae - FETi fast extensor tibiae motor neurone - FlTi flexor tibiae - pCS posterior campaniform sensillum     

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.     

Octopaminergic modulation of locust motor neurones

The effect of octopamine on the fast extensor and the flexor tibiae motor neurones in the locust (Schistocerca gregaria) metathoracic ganglion, and also on synaptic transmission from the fast extensor to the flexor motor neurones, was examined. Bath application or ionophoresis of octopamine depolarized and increased the excitability of the flexor tibiae motor neurones. 1 mM octopamine reduced the amplitude of the fast extensor-evoked EPSP in the slow but not the fast flexor motor neurones, whereas 10 mM octopamine could reduce the EPSP amplitude in both. Octopamine broadened the fast extensor action potential and reduced the amplitude of the afterhyperpolarization, the modulation requiring feedback resulting from movement of the tibia. Octopamine also increased the frequency of synaptic inputs onto the tibial motor neurones, and could cause rhythmic activity in the flexor motor neurones, and reciprocal activity in flexor and extensor motor neurones. Octopamine also increased the frequency of spontaneous spiking in the octopaminergic dorsal unpaired median neurones. Repetitive stimulation of unidentified dorsal unpaired median neurones could mimic some of the effects of octopamine. However, no synaptic connections were found between dorsal unpaired median neurones and the tibial motor neurones. The diverse effects of octopamine support its role in mediating arousal.     

The mechanics of elevation control in locust jumping

How do animals control the trajectory of ballistic motions like jumping? Targeted jumps by a locust, which are powered by a rapid extension of the tibiae of both hind legs, require control of the take-off angle and speed. To determine how the locust controls these parameters, we used high speed images of jumps and mechanical analysis to reach three conclusions: (1) the extensor tibiae muscle applies equal and opposite torques to the femur and tibia, which ensures that tibial extension accelerates the centre of mass of the body along a straight line; (2) this line is parallel to a line drawn from the distal end of the tibia through the proximal end of the femur; (3) the slope of this line (the angle of elevation) is not affected if the two hind legs extend asynchronously. The mechanics thus uncouple the control of elevation and speed, allowing simplified and independent control mechanisms. Jump elevation is controlled mechanically by the initial positions of the hind legs and jump speed is determined by the energy stored within their elastic processes, which allows us to then propose which proprioceptors are involved in controlling these quantities.     

Physiological Recordings of High and Low Output NMJs on the Crayfish Leg Extensor Muscle

We explain in detail how to expose and conduct electrophysiological recordings of synaptic responses for high (phasic) and low (tonic) output motor neurons innervating the extensor muscle in the walking leg of a crayfish. Distinct differences are present in the physiology and morphology of the phasic and tonic nerve terminals. The tonic axon contains many more mitochondria, enabling it to take a vital stain more intensely than the phasic axon. The tonic terminals have varicosities, and the phasic terminal is filiform. The tonic terminals are low in synaptic efficacy but show dramatic facilitated responses. In contrast, the phasic terminals are high in quantal efficacy but show synaptic depression with high frequency stimulation. The quantal output is measured with a focal macropatch electrode placed directly over the visualized nerve terminals. Both phasic and tonic terminals innervate the same muscle fibers, which suggests that inherent differences in the neurons, rather than differential retrograde feedback from the muscle, account for the morphological and physiological differentiation.Download video file.^{(61M, mov)}     

Synaptic responses produced in lobster abdominal postural motor neurons by mechanical stimulation of the swimmeret

1. Intracellular recordings were obtained from the somata of identified abdominal postural motor neurons in lobster to examine their subthreshold and suprathreshold responses to tactile stimulation of the swimmeret. 2. Pressure stimulation of the swimmeret surface evoked abdominal extension by producing tonic spiking in the extensor excitors and the synergistic flexor inhibitor (f5) and hyperpolarizing responses in the extensor inhibitor and antagonistic flexor excitors. These responses often continued for several seconds following the termination of the stimulus. The receptive fields of these motor responses extended over most of the swimmeret surface. 3. More localized tactile stimulation of the swimmeret surface elicited EPSPs in f5 and the extensor excitors, and IPSPs in the flexor excitors. The amplitude of these synaptic potentials decreased as the stimulus intensity was reduced. 4. Stimulation of feathered hair (both sexes) and smooth hair (female only) sensilla produced responses characteristic of extension whereas bristly spines on the male accessory lobe excited only two flexor excitors without affecting any of the other postural motor neurons. 5. Summed synaptic responses recorded from the motor neurons differed in their amplitudes and latencies according to the type of mechanoreceptor stimulated-cuticular receptors, feathered hairs or smooth hairs. Stimulation of the swimmeret cuticle produced the strongest responses (shortest latency, largest amplitude), while feathered hair stimulation initiated the weakest responses (longest latency, smallest amplitude). 6. The relatively long latencies (greater than 35 ms) and the complex form of the EPSPs and IPSPs indicate the involvement of multisynaptic interneuronal pathways in the reflex arcs.     

The neural basis of catalepsy in the stick insect cuniculina impigra

The femur-tibia control system which is responsible for catalepsy is studied in the open-loop configuration (input: stimulation of the femoral chordotonal organ; output: spike-frequency of FETi and SETi as well as the force produced by the extensor tibiae muscle). Comparison of motor neuron activities and muscle force reveals the input-output relationships of the extensor tibiae muscle. This muscle behaves like a low-pass filter with a small time constant for rising inputs and a large time constant for falling inputs. It forms the decisive low-pass filter for force production of the complete system. For freely moving tibia, the elastic properties of the muscles combined with the inert mass of the tibia contribute to the low-pass filter properties. The muscle does not contribute to the high-pass filter properties of the complete system. During repetitive stimulation FETi habituates quickly.Supported by DFG Ba 578     

Neural circuits for jumping in the locust

The locust jump consists of three distinct phases: Cocking: a rapid flexion of both hindleg tibia and locking of both tibia in full flexion. Co-contraction: simultaneous contractions in hindleg flexor and extensor muscles lasting about 0.5 s resulting in the storage of energy for the jump in elastic elements of the legs and muscles. Triggering: a sudden inhibition of flexor activity to allow the shortening of the contracted extensors and the release of the energy stored during the co-contraction phase. The neural circuitry controlling these three phases is now reasonably well understood. Some of its major features are: (1) pairs of large identifiable interneurons in the thoracic ganglia for evoking the cocking response (C-neurons) and for triggering the jump (M-neurons), (2) a central excitatory pathway from extensor to flexor tibiae motoneurons to ensure simultaneous activation of extensor and flexor motoneurons during the initial part of the co-contraction phase, (3) a positive feedback pathway from cuticular receptors to extensor motoneurons for maintaining extensor activity during the co-contraction phase, (4) proprioceptive feedback to the trigger interneurons for increasing their excitability during the co-contraction phase and thereby allowing a variety of external stimuli to activate the trigger neurons and evoke a jump, (5) presynaptic inhibition of visual pathways to the trigger neurons to ensure that the trigger neurons are not activated by the simultaneous occurrence of visual and auditory stimuli in the absence of proprioceptive input, and (6) a pair of multifunctional visual movement detecting neurons which can initiate cocking or trigger the jump depending on the animal's state.     

Sense organs in the femur of the stick insect and their relevance to the control of position of the femur-tibia-joint

Summary The sensory innervation pattern is described for the femur of the middle and the hind legs ofCarausius morosus. — In one of the nerves (F121) extracellular recordings show a unit which mirrors the tension of the flexor tibiae muscle (tension receptor). The tension receptor increases the firing rate of the slow extensor tibiae motoneuron. It measures the tension of one or more muscle fibres of the anterior side near the distal end of the muscle. The anatomical basis of this receptor is uncertain. — Another receptor was found on the ventral side of the distal end of the apodeme of the extensor tibiae muscle (apodeme receptor). Recordings from this receptor could not be obtained inCarausius. But inExtatosoma tiaratum it responded to stretching of the nerve. In the natural position it shows a minimum of excitation in the 90°-position of the femur-tibia-joint and an increase in firing rate for both flexion and extension. — Tactile hairs react phasically and have no special sensitivity for one direction. Two receptors at the dorsal side of the femur-tibia-joint (RDAL and RDPL), which are situated in the same position as inSchistocerca hind legs, react phasically to extension movements and fire tonically in the most extended position of the joint. — The influence of these receptors on the position of the femur-tibia-joint is only weak.Supported by Deutsche Forschungsgemeinschaft     

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.     

The energetics of the jump of the locust Schistocerca gregaria.

The anatomy of the metathoracic leg is redescribed with particular reference to storage of energy in cuticular elements and the way in which the stored energy is used in jumping. The jump of adult male locusts requires an energy of 9 mJ and that of the female requires 11 mJ. The semilunar processes of each metafemur store 4 mJ at a stress of 15 N, and the extensor tibiae apodeme stores a further 3 mJ at the same stress. The total stored energy in both metathoracic legs is 14 mJ. The extensor tibiae muscle produces a maximum isometric force of over 15 N at 30 degrees C and, when loaded with the extensor apodeme and semilunar processes, attains this force in 0.3 sec with a strain of 0.8 mm. The peak power output is 36 mW or 0.45 W.g-1. The peak isometric force is attained when the tibia is fully flexed and the force falls as the tibia extends. The extensor tibiae muscle A band is 5.5 mum long and the peak force is over 0.75 N.m-2. The peak velocity of shortening is 7 mm.sec-1 or about 1.75 lengths/sec at 30 degrees C. The tensile strength of the extensor apodeme is 0.6 kN.mm-2 and Young's modulus is 19 kN.mm-2. The safety factor does not exceed 1.2 and the safety factor of the semilunar processes and tibial cuticle is little higher. The jump impulse lasts 25-30 msec. A velocity of 3.2 m.sec-1 is reached after a peak acceleration of 180 m.sec-2. The peak power output is 0.75 W at close to maximum velocity. Energy losses in rotating the femur and tibia are small and it is shown that the leg is able to extend at 7 times the normal rate with losses of about 20%. Most of the stored energy is converted to kinetic energy as the animal jumps. A model is based on the relaxation of a spring that has the properties of the elastic elements of the locust leg into a lever with the same kinematics as the locust leg produces a force-distance curve similar to that measured for locust jumps. The major part of the jump energy is stored before the jump.