A central pattern-generating network contributes to "reflex-reversal"-like leg motoneuron activity in the locust.

We introduce a new rhythmic preparation of the locust mesothoracic segment that exhibits long-lasting rhythmicity without pharmacological treatment. In most experiments, isolation of the locust mesothoracic ganglion from the anterior and posterior ganglia causes episodes of patterned activity to be generated in leg motoneurons that supply the femur-tibia (FT) joint. Flexor and extensor tibiae motoneuron pools exhibit alternating bursts of activity mostly composed of doublets and triplets of bursts. Motor activity during these episodes appears to be centrally generated because it persisted after complete deafferentation in 37% of the preparations; however, proprioceptive signals from the middle leg strongly influenced the patterning of motoneuron activity. Mimicking FT joint flexion by elongating the femoral chordotonal organ during an extensor burst terminates extensor activity and initiates flexor activity. The reverse is true for a mimicked extension during a flexor burst. This motor activity represents a reflex reversal that is typically observed in the locomotor state of the stick insect walking system. Our results provide evidence that this "reversed" reflex is caused by the action of central pattern-generating networks.

The role of sensory signals from the insect coxa-trochanteral joint in controlling motor activity of the femur-tibia joint.

Interjoint coordination in multi-jointed limbs is essential for the generation of functional locomotor patterns. Here we have focused on the role that sensory signals from the coxa-trochanteral (CT) joint play in patterning motoneuronal activity of the femur-tibia (FT) joint in the stick insect middle leg. This question is of interest because when the locomotor system is active, movement signals from the FT joint are known to contribute to patterning of activity of the central rhythm-generating networks governing the CT joint. We investigated the influence of femoral levation and depression on the activity of tibial motoneurons. When the locomotor system was active, levation of the femur often induced a decrease or inactivation of tibial extensor activity while flexor motoneurons were activated. Depression of the femur had no systematic influence on tibial motoneurons. Ablation experiments revealed that this interjoint influence was not mediated by signals from movement and/or position sensitive receptors at the CT joint, i.e., trochanteral hairplate, rhombal hairplate, or internal levator receptor organ. Instead the influence was initiated by sensory signals from a field of campaniform sensillae, situated on the proximal femur (fCS). Selective stimulation of these fCS produced barrages of inhibitory postsynaptic potentials (IPSPs) in tibial extensor motoneurons and activated tibial flexor motoneurons. During pharmacologically activated rhythmic activity of the otherwise isolated mesothoracic ganglion (pilocarpine, 5 x 10(-4) M), deafferented except for the CT joint, levation of the femur as well had an inhibitory influence on tibial extensor motoneurons. However, the influence of femoral levation on the rhythm generated was rather labile and only sometimes a reset of the rhythm was induced. In none of the preparations could entrainment of rhythmicity by femoral movement be achieved, suggesting that sensory signals from the CT joint only weakly affect central rhythm-generating networks of the FT joint. Finally, we analyzed the role of sensory signals from the fCS during walking by recording motoneuronal activity in the single middle leg preparation with fCS intact and after their removal. These experiments showed that fCS activity plays an important role in generating tibial motoneuron activity during the stance phase of walking.

Pattern generation for walking and searching movements of a stick insect leg. II. Control of motoneuronal activity.

In the stick insect, Cuniculina impigra, intracellular recordings from mesothoracic motoneurons that control flexion and extension of the tibia and depression and levation of the trochantero-femur were made while the leg performed walking-like movements on a treadband or stereotyped rhythmic searching movements. We were interested in how synaptic input and intrinsic properties contribute to form the activity pattern of motoneurons during rhythmic leg movements without sensory feedback from other legs. During searching and walking, motoneurons expressed a rhythmic bursting pattern that was formed by a depolarizing input followed by a hyperpolarizing input in the inter-burst interval. This basic pattern was similar in all fast, semi-fast, and slow motoneurons that were recorded. Hyperpolarizations were in synchrony with activity in the antagonistic motoneurons. De- and hyperpolarizations were associated with a decrease in input resistance. All motoneurons showed spike frequency adaptation when depolarized by current injection to a membrane potential similar to that observed during walking. In the hyperpolarizing phase of fast flexor motoneurons, the initial maximum hyperpolarization was followed by a sag in potential toward more depolarized values. Consistent with this observation, only fast flexor motoneurons developed a depolarizing sag potential when hyperpolarized by injection of constant negative current.

Pattern generation for walking and searching movements of a stick insect leg. I. Coordination of motor activity.

During walking, the six legs of a stick insect can be coordinated in different temporal sequences or gaits. Leg coordination in each gait is controlled and stabilized by coordinating mechanisms that affect the action of the segmental neuronal networks for walking pattern generation. At present, the motor program for single walking legs in the absence of movement-related coordinating intersegmental influences from the other legs is not known. This knowledge is a prerequisite for the investigation of the segmental neuronal mechanisms that control the movements of a leg and to study the effects of intersegmental coordinating input. A stick insect single middle leg walking preparation has been established that is able to actively perform walking movements on a treadband. The walking pattern showed a clear division into stance and swing phases and, in the absence of ground contact, the leg performed searching movements. We describe the activity patterns of the leg muscles and motoneurons supplying the coxa-trochanteral joint, the femur-tibial joint, and the tarsal leg joints of the middle leg during both walking and searching movements. Furthermore we describe the temporal coordination between them. During walking movements, the coupling between the leg joints was phase-constant; in contrast during searching movements, the coupling between the leg joints was dependent on cycle period. The motor pattern of the single leg generated during walking exhibits similarities with the motor pattern generated during a tripod gait in an intact animal. The generation of walking movements also drives the activity of thoraco-coxal motoneurons of the deafferented and de-efferented thoraco-coxal leg joint in a phase-locked manner, with protractor motoneurons being active during swing and retractor motoneurons being active during stance. These results show that for the single middle leg, a basic walking motor pattern is generated sharing similarities with the tripod gait and that the influence of the motor pattern generated in the distal leg joints is sufficient for driving the activity of coxal motoneurons so an overall motor pattern resembling forward walking is generated.

Roles of high-voltage-activated calcium channel subtypes in a vertebrate spinal locomotor network.

Lamprey spinal cord neurons possess N-, L-, and P/Q-type high-voltage-activated (HVA) calcium channels. We have analyzed the role of the different HVA calcium channels subtypes in the overall functioning of the spinal locomotor network by monitoring the influence of their specific agonists and antagonists on synaptic transmission and on N-methyl-D-aspartate (NMDA)-elicited fictive locomotion. The N-type calcium channel blocker omega-conotoxin GVIA (omega-CgTx) depressed synaptic transmission from excitatory and inhibitory interneurons. Blocking L-type and P/Q-type calcium channels with nimodipine and omega-agatoxin, respectively, did not affect synaptic transmission. Application of omega-CgTx initially decreased the frequency of the locomotor rhythm, increased the burst duration, and subsequently increased the coefficient of variation and disrupted the motor pattern. These effects were accompanied by a depression of the synaptic drive between neurons in the locomotor network. Blockade of L-type channels by nimodipine also decreased the frequency and increased the duration of the locomotor bursts. Conversely, potentiation of L-type channels increased the frequency of the locomotor activity and decreased the duration of the ventral root bursts. In contrast to blockade of N-type channels, blockade or potentiation of L-type calcium channels had no effect on the stability of the locomotor pattern. The P/Q-type calcium channel blocker omega-agatoxin IVA had little effect on the locomotor frequency or burst duration. The results indicate that rhythm generation in the spinal locomotor network of the lamprey relies on calcium influx through L-type and N-type calcium channels.

Neuromuscular plasticity in the locust after permanent removal of an excitatory motoneuron of the extensor tibiae muscle.

The capacity of the larval insect nervous system to compensate for the permanent loss of one of the two excitatory motoneurons innervating a leg muscle was investigated in the locust (Locusta migratoria). In the fourth instar, the fast extensor tibiae (FETi) motoneuron in the mesothoracic ganglion was permanently removed by photoinactivation with a helium-cadmium laser. Subsequently, the animals were allowed to develop into adulthood. When experimental animals were tested as adults after final ecdysis, fast-contracting fibers in the most proximal region of the corresponding extensor muscle, which are normally predominantly innervated by FETi only, uniformly responded to activity of the slow extensor tibiae (SETi) neuron. In adult operated animals, single pulses to SETi elicited large junctional responses in the fibers which resulted in twitch contractions of these fibers similar to the responses to FETi activity in control animals. The total number of muscle fibers, their properties as histochemically determined contractional types (fast and slow), and their distribution were not affected by photoinactivation of FETi. Possible mechanisms enabling the larval neuromuscular system to compensate for the loss of FETi through functionally similar innervation by a different motoneuron, i.e. SETi, are discussed.

Calcium channels involved in synaptic transmission from reticulospinal axons in lamprey.

The pharmacology of calcium channels involved in glutamatergic synaptic transmission from reticulospinal axons in the lamprey spinal cord was analyzed with specific agonists and antagonists of different high-voltage activated calcium channels. The N-type calcium channel blocker omega-conotoxin GVIA (omega-CgTx) induced a large decrease of the amplitude of reticulospinal-evoked excitatory postsynaptic potentials (EPSPs). The P/Q-type calcium channel blocker omega-agatoxin IVA (omega-Aga) also reduced the amplitude of the reticulospinal EPSPs, but to a lesser extent than omega-CgTx. The dihydropyridine agonist Bay K and antagonist nimodipine had no effect on the amplitude of the reticulospinal EPSP. Combined application of omega-CgTx and omega-Aga strongly decreased the amplitude the EPSPs but was never able to completely block them, indicating that calcium channels insensitive to these toxins (R-type) are also involved in synaptic transmission from reticulospinal axons. We have previously shown that the group III metabotropic glutamate receptor agonist L(+)-2-amino-4-phosphonobutyric acid (L-AP4) mediates presynaptic inhibition at the reticulospinal synapse. To test if this presynaptic effect is mediated through inhibition of calcium influx, the effect of L-AP4 on reticulospinal transmission was tested before and after blockade of N-type channels, which contribute predominantly to transmitter release at this synapse. Blocking the N-type channels with omega-CgTx did not prevent inhibition of reticulospinal synaptic transmission by L-AP4. In addition, L-AP4 had no affect on the calcium current recorded in the somata of reticulospinal neurons or on the calcium component of action potentials in reticulospinal axons. These results show that synaptic transmission from reticulospinal axons in the lamprey is mediated by calcium influx through N-, P/Q- and R-type channels, with N-type channels playing the major role. Furthermore, presynaptic inhibition of reticulospinal transmission by L-AP4 appears not to be mediated through inhibition of presynaptic calcium channels.

Role of proprioceptive signals from an insect femur-tibia joint in patterning motoneuronal activity of an adjacent leg joint.

Interjoint reflex function of the insect leg contributes to postural control at rest or to movement control during locomotor movements. In the stick insect (Carausius morosus), we investigated the role that sensory signals from the femoral chordotonal organ (fCO), the transducer of the femur-tibia (FT) joint, play in patterning motoneuronal activity in the adjacent coxa-trochanteral (CT) joint when the joint control networks are in the movement control mode of the active behavioral state. In the active behavioral state, sensory signals from the fCO induced transitions of activity between antagonistic motoneuron pools, i.e., the levator trochanteris and the depressor trochanteris motoneurons. As such, elongation of the fCO, signaling flexion of the FT joint, terminated depressor motoneuron activity and initiated activity in levator motoneurons. Relaxation of the fCO, signaling extension of the FT joint, induced the opposite transition by initiating depressor motoneuron activity and terminating levator motoneuron activity. This interjoint influence of sensory signals from the fCO was independent of the generation of the intrajoint reflex reversal in the FT joint, i.e., the "active reaction," which is released by elongation signals from the fCO. The generation of these transitions in activity of trochanteral motoneurons barely depended on position or velocity signals from the fCO. This contrasts with the situation in the resting behavioral state when interjoint reflex action markedly depends on actual fCO stimulus parameters, i.e., position and velocity signals. In the active behavioral state, movement signals from the fCO obviously trigger or release centrally generated transitions in motoneuron activity, e.g., by affecting central rhythm generating networks driving trochanteral motoneuron pools. This conclusion was tested by stimulating the fCO in "fictive rhythmic" preparations, activated by the muscarinic agonist pilocarpine in the otherwise isolated and deafferented mesothoracic ganglion. In this situation, sensory signals from the fCO did in fact reset and entrain rhythmic activity in trochanteral motoneurons. The results indicate for the first time that when the stick insect locomotor system is active, sensory signals from the proprioceptor of one leg joint, i.e., the fCO, pattern motor activity in an adjacent leg joint, i.e., the CT joint, by affecting the central rhythm generating network driving the motoneurons of the adjacent joint.

Phase-dependent presynaptic modulation of mechanosensory signals in the locust flight system.

In the locust flight system, afferents of a wing hinge mechanoreceptor, the hindwing tegula, make monosynaptic excitatory connections with motoneurons of the elevator muscles. During flight motor activity, the excitatory postsynaptic potentials (EPSPs) produced by these connections changed in amplitude with the phase of the wingbeat cycle. The largest changes occurred around the phase where elevator motoneurons passed through their minimum membrane potential. This phase-dependent modulation was neither due to flight-related oscillations in motoneuron membrane potential nor to changes in motoneuron input resistance. This indicates that modulation of EPSP amplitude is mediated by presynaptic mechanisms that affect the efficacy of afferent synaptic input. Primary afferent depolarizations (PADs) were recorded in the terminal arborizations of tegula afferents, presynaptic to elevator motoneurons in the same hemiganglion. PADs were attributed to presynaptic inhibitory input because they reduced the input resistance of the afferents and were sensitive to the gamma-aminobutyric acid antagonist picrotoxin. PADs occurred either spontaneously or were elicited by spike activity in the tegula afferents. In summary, afferent signaling in the locust flight system appears to be under presynaptic control, a candidate mechanism of which is presynaptic inhibition.

Inhibitory synaptic drive patterns motoneuronal activity in rhythmic preparations of isolated thoracic ganglia in the stick insect.

During active leg movements of an insect leg, the activity of the motoneuron pools of each individual leg joint is generated by the interaction between signals from central rhythm generating sources, peripheral signals as well as coordinating signals from other leg joints and legs. The nature of the synaptic drive from the central rhythm generators onto the motoneuron pools of the individual leg joints during rhythmic motor activity of the stick insect (Carausius morosus) middle leg has been investigated. In the isolated mesothoracic ganglion central rhythm generators were activated pharmacologically by topical application of the muscarinic agonist pilocarpine. Motoneurons supplying the femur-tibia (FT) joint were investigated in detail. Recordings from neuropil processes of these motoneurons revealed that patterning of their rhythmic activity is based on cyclic hyperpolarizing synaptic inputs. These inputs are in clear antiphase for extensor and flexor motoneurons. DCC (discontinuous current clamp) and dSEVC (discontinuous single electrode voltage clamp) recordings showed reversal potentials of the inhibitory inputs between -80 to -85 mV (FETi, N=7; Flex MN, N=3). After intracellular injection of TEA rhythmic inhibition in FETi was decreased by about 84% (N=4). Both findings indicate that the cyclic inhibition is mediated by potassium ions. Thus, it appears that central rhythm generators pattern motor activity in antagonistic tibial motoneuron pools by cyclic alternating inhibition.

Sensory pathways and their modulation in the control of locomotion.

Recent experiments have extended our understanding of how sensory information in premotor networks controlling motor output is processed during locomotion, and at what level the efficacy of specific sensory-motor pathways is determined. Phasic presynaptic inhibition of sensory transmission combined with postsynaptic alterations of excitatory and inhibitory synaptic transmission from interneurons of the premotor networks contribute to the modulation of reflex pathways and to the generation of reflex reversal. These mechanisms play an important role in adapting the operation of central networks to external demands and thus help optimize sensory-motor integration.

Sensorimotor pathways involved in interjoint reflex action of an insect leg.

Coordination of motor output between leg joints is crucial for the generation of posture and active movements in multijointed appendages of legged organisms. We investigated in the stick insect the information flow between the middle leg femoral chordotonal organ (fCO), which measures position and movement in the femur-tibia (FT) joint and the motoneuron pools supplying the next proximal leg joint, the coxa-trochanteral (CT) joint. In the inactive animal, elongation of the fCO (by flexing the FT joint) induced a depolarization in eight of nine levator trochanteris motoneurons, with a suprathreshold activation of one to three motoneurons. Motoneurons of the depressor trochanteris muscle were inhibited by fCO elongation. Relaxation signals, i.e., extension of the FT joint, activated both levator and depressor motoneurons; i.e., both antagonistic muscles were coactivated. Monosynaptic as well as polysynaptic pathways contribute to interjoint reflex actions in the stick insect leg. fCO afferents were found to induce short latency EPSPs in levator motoneurons, providing evidence for direct connections between fCO afferents and levator motoneurons. In addition, neuronal pathways via intercalated interneurons were identified that transmit sensory information from the fCO onto levator and/or depressor motoneurons. Finally, we describe two kinds of alterations in interjoint reflex action: (a) With repetitive sensory stimulation, this interjoint reflex action shows a habituation-like decrease in strength. (b) In the actively moving animal, interjoint reflex action in response to fCO elongation, mimicking joint flexion, qualitatively remained the same sign, but with a marked increase in strength, indicating an increased influence of sensory signals from the FT joint onto the adjacent CT joint in the active animal.

Plasticity of synaptic connections in sensory-motor pathways of the adult locust flight system.

We investigated possible roles of retrograde signals and competitive interactions in the lesion-induced reorganization of synaptic contacts in the locust CNS. Neuronal plasticity is elicited in the adult flight system by removal of afferents from the tegula, a mechanoreceptor organ at the base of the wing. We severed one hindwing organ and studied the resulting rearrangement of synaptic contacts between flight interneurons and afferent neurons from the remaining three tegulae (2 forewing, 1 hindwing). This was done by electric stimulation of afferents and intracellular recording from interneurons (and occasionally motoneurons). Two to three weeks after unilateral tegula lesion, connections between tegula afferents and flight interneurons were altered in the following way. 1) Axons from the forewing tegula on the operated side had established new synaptic contacts with metathoracic elevator interneurons. In addition, the amplitude of compound excitatory postsynaptic potentials elicited by electric stimulation was increased, indicating that a larger number of afferents connected to any given interneuron. 2) On the side contralateral to the lesion, connectivity between axons from the forewing tegula and elevator interneurons was decreased. 3) The efficacy of the (remaining) hindwing afferents appeared to be increased with regard to both synaptic transmission to interneurons and impact on flight motor pattern. 4) Flight motoneurons, which are normally restricted to the ipsilateral hemiganglion, sprouted across the ganglion midline after unilateral tegula removal and apparently established new synaptic contacts with tegula afferents on that side. The changes on the operated side are interpreted as occupation of synaptic space vacated on the interneurons by the severed hindwing afferents. On the contralateral side, the changes in synaptic contact must be elicited by retrograde signals from bilaterally arborizing flight interneurons, because tegula projections remain strictly ipsilateral. The pattern of changes suggests competitive interactions between forewing and hindwing afferents. The present investigation thus presents evidence that the CNS of the mature locust is capable of extensive synaptic rearrangement in response to injury and indicates for the first time the action of retrograde signals from interneurons.

Role of presynaptic inputs to proprioceptive afferents in tuning sensorimotor pathways of an insect joint control network.

The femur-tibia (FT) joint of insects is governed by a neuronal network that controls activity in tibial motoneurons by processing sensory information about tibial position and movement provided by afferents of the femoral chordotonal organ (fCO). We show that central arborizations of fCO afferents receive presynaptic depolarizing synaptic inputs. With an average resting potential of -71.9 +/- 3.72 mV (n = 10), the reversal potential of these potentials is on average -62.8 +/- 2.3 mV (n = 5). These synaptic potentials occur either spontaneously or are related to movements at the fCO. They are thus induced by signals from other fCO afferents. Therefore, the synaptic inputs to fCO afferents are specific and depend on the sensitivity of the individual afferent affected. These potentials reduce the amplitude of concurrent afferent action potentials. Bath application of picrotoxin, a noncompetitive blocker of chloride ion channels, blocks these potentials, which indicates that they are mediated by chloride ions. From these results, it is concluded that these are inhibitory synaptic potentials generated in the central terminals of fCO afferents. Pharmacologic removal of these potentials affects the tuning of the complete FT control system. Following removal, the dependence of the FT control loop on the tibia position increases relative to the dependency on the velocity of tibia movements. This is due to changes in the relative weighting of the position and velocity signals in the parallel interneuronal pathways from the fCO onto tibial motoneurons. Consequently, the FT joint is no longer able to perform twig mimesis (i.e., catalepsy), which is known to rely on a low position compared to the high-velocity dependency of the FT control system.

Premotor interneurons in generation of adaptive leg reflexes and voluntary movements in stick insects.

We investigated the role of local nonspiking interneurons involved in motor control of legs in the stick insects, Carausius morosus. In a preparation that allowed the animals to perform active leg movements such as adaptive tactile reflexes, proprioceptive reflexes, and walking, we gathered the following results. Almost all tested nonspiking interneurons that provide synaptic drive onto moto-neurons of the proximal leg muscles contribute to all of the motor programs underlying tactile reflexes and voluntary leg movements such as walking, searching, and rocking. Most of them are also involved in the generation of proprioceptive reflexes. All motor programs for coactivation, avoidance reflexes, resistance reflexes, and voluntary leg movements result from parallel pathways including nonspiking interneurons that support and others that oppose the motoneuronal activity. The contribution of a single interneuron to the different motor program is specific: it can be supporting for one motor program but opposing for the other. Even for the same motor program, for example, coactivation, the contribution of an individual interneuron can depend on the stimulus site from where the response is elicited. Our results support the idea that the different motor patterns for adaptive tactile reflexes, resistance reflexes, and voluntary leg movements emerge from a multifunctional neuronal circuit that is reorganized corresponding to the motor behavior performed. The actual motor pattern is then shaped by distributed information processing in parallel supporting and opposing pathways.

Distributed processing on the basis of parallel and antagonistic pathways simulation of the femur-tibia control system in the stick insect.

In inactive stick insects, sensory information from the femoral chordotonal organ (fCO) about position and movement of the femur-tibia joint is transferred via local nonspiking interneurons onto extensor and flexor tibiae motoneurons. Information is processed by the interaction of antagonistic parallel pathways at two levels: (1) at the input side of the nonspiking interneurons and (2) at the input side of the motoneurons. We tested by a combination of physiological experiments and computer simulation whether the known network topology and the properties of its elements are sufficient to explain the generation of the motor output in response to passive joint movements, that is resistance reflexes. In reinvestigating the quantitative characteristics of interneuronal pathways we identified 10 distinct types of nonspiking interneurons. Synaptic inputs from fCO afferents onto these interneurons are direct excitatory and indirect inhibitory. These connections were investigated with respect to position and velocity signals from the fCO. The results were introduced in the network simulation. The motor output of the simulation has the same characteristics as the real system, even when particular types of interneurons were removed in the simulation and the real system.

Role of local nonspiking interneurons in the generation of rhythmic motor activity in the stick insect.

Local nonspiking interneurons in the thoracic ganglia of insects are important premotor elements in posture control and locomotion. It was investigated whether these interneurons are involved in the central neuronal circuits generating the oscillatory motor output of the leg muscle system during rhythmic motor activity. Intracellular recordings from premotor nonspiking interneurons were made in the isolated and completely deafferented mesothoracic ganglion of the stick insect in preparations exhibiting rhythmic motor activity induced by the muscarinic agonist pilocarpine. All interneurons investigated provided synaptic drive to one or more motoneuron pools supplying the three proximal leg joints, that is, the thoraco-coxal joint, the coxa-trochanteral joint and the femur-tibia joint. During rhythmicity in 83% (n = 67) of the recorded interneurons, three different kinds of synaptic oscillations in membrane potential were observed: (1) Oscillations were closely correlated with the activity of motoneuron pools affected; (2) membrane potential oscillations reflected only certain aspects of motoneuronal rhythmicity; and (3) membrane potential oscillations were correlated mainly with the occurrence of spontaneous recurrent patterns (SRP) of activity in the motoneuron pools. In individual interneurons membrane potential oscillations were associated with phase-dependent changes in the neuron's membrane conductance. Artificial changes in the interneurons' membrane potential strongly influenced motor activity. Injecting current pulses into individual interneurons caused a reset of rhythmicity in motoneurons. Furthermore, current injection into interneurons influenced shape and probability of occurrence for SRPs. Among others, identified nonspiking interneurons that are involved in posture control of leg joints were found to exhibit the above properties. From these results, the following conclusions on the role of nonspiking interneurons in the generation of rhythmic motor activity, and thus potentially also during locomotion, emerge: (1) During rhythmic motor activity most nonspiking interneurons receive strong synaptic drive from central rhythm-generating networks; and (2) individual nonspiking interneurons some of which underlie sensory-motor pathways in posture control, are elements of central neuronal networks that generate alternating activity in antagonistic leg motoneuron pools.

Nonspiking local interneurons in insect leg motor control. I. Common layout and species-specific response properties of femur-tibia joint control pathways in stick insect and locust.

1. Locusts (Locusta migratoria) and stick insects (Carausius morosus) exhibit different strategies for predator avoidance. Locusts rely primarily on walking and jumping to evade predators, whereas stick insects become cataleptic, catalepsy forming a major component of the twig mimesis exhibited by this species. The neuronal networks that control postural leg movements in locusts and stick insects are tuned differently to their specific behavioral tasks. An important prerequisite for the production of catalepsy in the stick insect is the marked velocity dependency of the control network, which appears to be generated at the level of nonspiking local interneurons. We examined interneuronal pathways in the network controlling the femur-tibia joint of the locust middle leg and compared its properties with those described for the stick insect middle leg. It was our aim to identify possible neural correlates of the species-specific behavior with regard to postural leg motor control. 2. We obtained evidence that the neuronal networks that control the femur-tibia joints in the two species consist of morphologically and physiologically similar--and thus probably homologous--interneurons. Qualitatively, these interneurons receive the same input from the femoral chordotonal organ receptors and they drive the same pools of leg motoneurons in both species. 3. Pathways that contribute to the control of the femur-tibia joint include interneurons that support both "resisting" and "assisting" responses with respect to the motoneuron activity that is actually elicited during reflex movements. Signal processing via parallel, antagonistic pathways therefore appears to be a common principle in insect leg motor control. 4. Differences between the two insect species were found with regard to the processing of velocity information provided by the femoral chordotonal organ. Interneuronal pathways are sensitive to stimulus velocity in both species. However, in the locust there is no marked velocity dependency of the interneuronal responses, whereas in the same interneurons of the stick insect it is pronounced. This characteristic was maintained at the level of the motoneurons controlling the femur-tibia joint. Pathways for postural leg motor control in the locust thus lack an important prerequisite for the generation of catalepsy, that is, a marked velocity dependency.

Nonspiking local interneurons in insect leg motor control. II. Role of nonspiking local interneurons in the control of leg swing during walking.

1. Nonspiking local interneurons (NSIs) were recorded intracellularly in the mesothoracic ganglion of semi-intact locusts walking on a treadwheel. Interneurons were characterized by their connectivity to motoneurons. Their activity patterns in the step cycle and the effect current injection had on the leg movement were analyzed. We examined interneurons that provided excitatory or inhibitory synaptic drive to a subset of motoneurons active during the swing movement of walking. 2. Interneuron activity was observed to support or oppose the actual leg movement. Both supporting and opposing interneurons were active simultaneously, lending support to the idea that the actual motor output of walking is generated by the adjustment of parallel antagonistic pathways of signal processing. 3. The examined interneurons showed qualitatively the same patterns of activity during forward and backward walking. This indicates that swing movement in both situations may be generated by similar neuronal networks (although the mechanism of movement reversal remains unclear). 4. At least two functional types of NSIs could be distinguished. First, there were interneurons whose depolarization patterns showed distinct variability, often correlated with duration or amplitude of the swing movement. As a rule, current injection had minor, if any, effects on leg movement. Populations of these interneurons appear to be involved in the control of a coordinated swing movement by driving appropriate sets of muscle groups. The second type of NSIs showed more stereotyped activity patterns that varied relatively little with changes in the swing movement. Current injection had strong effects on the leg movement and could, for example, arrest the leg in the stance phase. These interneurons appear to be primarily involved in the trigger mechanism of leg swing.