Intersegmental transfer of sensory signals in the stick insect leg muscle control system

Intersegmental coordination during locomotion in legged animals arises from mechanical couplings and the exchange of neuronal information between legs. Here, the information flow from a single leg sense organ of the stick insect Cuniculina impigra onto motoneurons and interneurons of other legs was investigated. The femoral chordotonal organ (fCO) of the right middle leg, which measures posture and movement of the femur-tibia joint, was stimulated, and the responses of the tibial motoneuron pools of the other legs were recorded. In resting animals, fCO signals did not affect motoneuronal activity in neighboring legs. When the locomotor system was activated and antagonistic motoneurons were bursting in alternation, fCO stimuli facilitated transitions from flexor to extensor activity and vice versa in the contralateral leg. Following pharmacological treatment with picrotoxin, a blocker of GABA-ergic inhibition, the tibial motoneurons of all legs showed specific responses to signals from the middle leg fCO. For the contralateral middle leg we show that fCO signals encoding velocity and position of the tibia were processed by those identified local premotor nonspiking interneurons known to contribute to posture and movement control during standing and voluntary leg movements. Interneurons received both excitatory and inhibitory inputs, so that the response of some interneurons supported the motoneuronal output, while others opposed it. Our results demonstrate that sensory information from the fCO specifically affects the motoneuronal activity of other legs and that the layer of premotor nonspiking interneurons is a site of interaction between local proprioceptive sensory signals and proprioceptive signals from other legs.     

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. © 1997 John Wiley & Sons, Inc. J Neurobiol 33: 891–913, 1997     

Physiological changes in central neuronal pathways contributing to the generation of a reflex reversal

1. In the stick insect Carausius morosus the properties of the neuronal network governing the femur-tibia joint depend on the behavioral state of the animal. In the inactive animal flexion of the femur-tibia joint results in the generation of a resistance reflex, while in the active animal the same stimulus induces the so-called active reaction, the first part of which is a reflex reversal.
2. Recordings from motoneurons innervating the extensor tibiae muscle indicated that their time course of activity during the active reaction is due to inputs from intercalated pathways. We therefore investigated the role of identified nonspiking interneurons that transmit sensory information from the chordotonal organ onto the extensor motoneurons in the inactive animal. We can show that (i) the nonspiking interneurons received altered inputs whereas (ii) they provided qualitatively the same synaptic drive onto leg motoneurons.
3. From our results it is clear that (i) neuronal pathways contributing to the generation of the resistance reflex are also involved in the generation of the reflex reversal in the same control loop, (ii) thereby adopting the same principle of information processing (parliamentary principle), because both, supporting and opposing pathways contribute to the generation of the motor output.

     

Information processing in the femur-tibia control loop of stick insects

The complicated response characteristics of the identified nonspiking interneuron type E4 upon elongation stimuli to the femoral chordotonal organ (fCO) can be obtained by a computer simulation using the neuronal network simulator BioSim, if the following assumptions were introduced: (1) The interneurons receive direct excitatory input from position- and velocity-sensitive fCO afferents but also, in parallel delayed inhibition from the same velocity-sensitive afferents. (2) Position-sensitive afferents in part show adaptation with a rather long time-constant. A subsequent experimental analysis demonstrated that all these assumptions fit the reality: (1) Interneurons of type E4 receive direct excitatory input from fCO afferents. (2) Interneurons of type E4 are affected by velocity dependent delayed inhibitory inputs from the fCO. (3) The fCO does contain adapting position-sensitive sensory neurons, which have not been described before. The described principle of the information processing is also able to generate the response in interneurons of type E6 with less steep amplitude-velocity characteristic due to a different weighting of the direct excitation and delayed inhibition.Abbreviations EPSP excitatory postsynaptic potential - FETi fast extensor tibiae motor neuron - fCO femoral chordotonal organ - FT-control loop femur-tibia control loop - IPSP inhibitory postsynaptic potential - SETi slow extensor tibiae motor neuron     

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. © 1995 John Wiley & Sons, Inc.     

Multiple gate control of the descending statocyst-motor pathway in the crayfish Procambarus clarkii Girard

1. Synaptic responses of uropod motoneurons and interneurons to magnetic field stimulation of the statocyst were studied in a whole animal preparation using intracellular recording and staining techniques to characterize the descending statocyst pathways controlling uropod steering behavior. 2. When the animal was engaged in abdominal postural movement, all uropod motoneurons received sustained excitatory input. Motoneurons which were to be activated during steering behavior showed excitatory responses to the stimulus superimposed on the sustained excitation. In the resting state, they showed weaker responses or no visible responses to the same stimulation. 3. Motoneurons to be suppressed during steering showed inhibitory responses to the stimulus only during abdominal movement. These included both active inhibition as well as disfacilitatory suppression of excitatory input to the motoneurons. 4. Premotor nonspiking interneurons, like motoneurons, showed greater responses to the stimulus during abdominal movement than at rest. Unlike motoneurons, however, they did not always receive sustained input during abdominal movement. 5. Descending axons which responded to statocyst stimulation independent of abdominal movement were found in the 4th and 5th abdominal ganglia. Other axons showed greater responses during abdominal movement than at rest. 6. A number of intersegmental descending interneurons with cell bodies and dendrites in the 4th or 5th ganglion were found to receive excitatory inputs from both the statocyst and the motor system controlling abdominal posture. These responses were found to summate with each other to generate spikes. 7. Statocyst signals are thus transmitted to uropod motoneurons by two types of descending pathways: one whose operation is affected by the abdominal system and the other which operates independently. The former pathway functions by recruiting intersegmental abdominal interneurons and makes stronger connections with motoneurons than the latter.     

Identified nonspiking interneurons in leg reflexes and during walking in the stick insect

In the stick insect Carausius morosus identified nonspiking interneurons (type E4) were investigated in the mesothoracic ganglion during intraand intersegmental reflexes and during searching and walking.In the standing and in the actively moving animal interneurons of type E4 drive the excitatory extensor tibiae motoneurons, up to four excitatory protractor coxae motoneurons, and the common inhibitor 1 motoneuron (Figs. 1–4).In the standing animal a depolarization of this type of interneuron is induced by tactile stimuli to the tarsi of the ipsilateral front, middle and hind legs (Fig. 5). This response precedes and accompanies the observed activation of the affected middle leg motoneurons. The same is true when compensatory leg placement reflexes are elicited by tactile stimuli given to the tarsi of the legs (Fig. 6).During forward walking the membrane potential of interneurons of type E4 is strongly modulated in the step-cycle (Figs.8–10). The peak depolarization occurs at the transition from stance to swing. The oscillations in membrane potential are correlated with the activity profile of the extensor motoneurons and the common inhibitor 1 (Fig. 9).The described properties of interneuron type E4 in the actively behaving animal show that these interneurons are involved in the organization and coordination of the motor output of the proximal leg joints during reflex movements and during walking.Abbreviations CLP reflex, compensatory leg placement reflex - CI1 common inhibitor I motoneuron - fCO femoral chordotonal organ - FETi fast extensor tibiae motoneuron - FT femur-tibia - SETi slow extensor tibiae motoneuron     

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. © 1997 John Wiley & Sons, Inc. J Neurobiol 32: 359–376, 1997.     

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 insect, 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 motoneurons 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 programs 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. © 1996 John Wiley & Sons, Inc.     

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.     

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     

Dendritic properties of uropod motoneurons and premotor nonspiking interneurons in the crayfish Procambarus clarkii Girard

Dendritic properties of uropod motoneurons and premotor nonspiking interneurons of crayfish have been studied using intradendritic recording and current injection. The input resistance of phasic motoneurons (5.20 ± 0.5 M; mean ± standard error) measured by injecting constant hyperpolarizing current was significantly lower than that of tonic motoneurons (10.3 ± 2.6 M; 0.02 < P < 0.05). The membrane time constant of phasic motoneurons (7.3 ± 0.9 ms) was also significantly shorter than that of tonic motoneurons (24.3 ± 2.5 ms; P < 0.001). Both types of motoneurons behaved linearly during hyperpolarization and sub-threshold depolarization. Nonspiking interneurons showed outward rectification upon depolarization. During hyperpolarization, their membrane behaved linearly and showed significantly higher input resistance (19.5 ± 2.5 M) than phasic and tonic motoneurons (P < 0.001). Their membrane time constant (38.0 ± 5.7 ms) was significantly longer than that of phasic motoneurons (P < 0.001) but not than that of tonic motoneurons (P > 0.05). In response to intracellular injection of sinusoidally oscillating current, phasic motoneurons showed one or two spikes per depolarization period irrespective of oscillating frequency ranging from 1 to 16 Hz. Tonic motoneurons showed larger numbers of spikes per stimulus period at lower frequencies. Nonspiking interneurons also showed phase-locked effects on the motoneuron spike activity. The effective frequency range over which injected oscillating current could modulate motoneuron spike activity was similar for tonic motoneurons and nonspiking interneurons.     

Intersegmental coordination in the lamprey: simulations using a network model without segmental boundaries

Swimming in vertebrates such as eel and lamprey involves the coordination of alternating left and right activity in each segment. Forward swimming is achieved by a lag between the onset of activity in consecutive segments rostrocaudally along the spinal cord. The intersegmental phase lag is approximately 1% of the cycle duration per segment and is independent of the swimming frequency. Since the lamprey has approximately 100 spinal segments, at any given time one wave of activity is propagated along the body. Most previous simulations of intersegmental coordination in the lamprey have treated the cord as a chain of coupled oscillators or well-defined segments. Here a network model without segmental boundaries is described which can produce coordinated activity with a phase lag. This ‘continuous’ pattern-generating network is composed of a column of 420 excitatory interneurons (E1 to E420) and 300 inhibitory interneurons (C1 to C300) on each half of the simulated spinal cord. The interneurons are distributed evenly along the simulated spinal cord, and their connectivity is chosen to reflect the behavior of the intact animal and what is known about the length and strength of the synaptic connections. For example, E100 connects to all interneurons between E51 and E149, but at varying synaptic strengths, while E101 connects to all interneurons between E52 and E150. This unsegmented E-C network generates a motor pattern that is sampled by output elements similar to motoneurons (M cells), which are arranged along the cell column so that they receive input from seven E and five C interneurons. The M cells thus represent the summed excitatory and inhibitory input at different points along the simulated spinal cord and can be regarded as representing the ventral root output to the myotomes along the spinal cord. E and C interneurons have five simulated compartments and Hodgkin-Huxley based dynamics. The simulated network produces rhythmic output over a wide range of frequencies (1–11 Hz) with a phase lag constant over most of the length, with the exception of the ‘cut’ ends due to reduced synaptic input. As the inhibitory C interneurons in the simulation have more extensive caudal than rostral projections, the output of the simulation has positive phase lags, as occurs in forward swimming. However, unlike the biological network, phase lags in the simulation increase significantly with burst frequency, from 0.5% to 2.3% over the range of frequencies of the simulation. Local rostral or caudal increases in excitatory drive in the simulated network are sufficient to produce motor patterns with increased or decreased phase lags, respectively. Received: 15 December 1995 / Accepted in revised form: 17 September 1996     

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     

Intracellular recordings from nonspiking interneurons in a semiintact, tethered walking insect.

Nonspiking interneurons were investigated in a tethered, walking insect, Carausius morosus, that was able to freely perform walking movements. Experiments were carried out with animals walking on a lightweight, double-wheel treadmill. Although the animal was opened dorsally, the walking system was left intact. Intracellular recordings were obtained from the dorsal posterior neuropil of the mesothoracic ganglion. Nonspiking interneurons, in which modulations of the membrane potential were correlated with the walking rhythm, were described physiologically and stained with Lucifer Yellow. Interneurons are demonstrated in which membrane potential oscillations mirror the leg position or show correlation with the motoneuronal activity of the protractor and retractor coxae muscles during walking. Other interneurons showed distinct hyperpolarizations at certain important trigger points in the step cycle, for example, at the extreme posterior position. Through electrical stimulation of single, nonspiking interneurons during walking, the motoneuronal activity in two antagonistic muscles--protractor and retractor coxae--could be reversed and even the movement of the ipsilateral leg could be influenced. The nonspiking interneurons described appear to be important premotor elements involved in walking. They receive, integrate, and process information from different leg proprioceptors and drive groups of leg motoneurons during walking.     

Effects of leg movements on the synaptic activity of descending statocyst interneurons in crayfish,Procambarus clarkii

Crustacean postural control is modulated by behavioral condition. In this study, we investigated how the responses of descending statocyst interneurons were affected during leg movements. Intracellular recording was made from an animal whose statoliths had been replaced with ferrite grains so that statocyst receptors could be activated by magnetic field stimulation. We identified 14 morphological types of statocyst-driven descending interneurons. Statocyst-driven descending interneurons always showed an excitatory response to statocyst stimulation on either ipsilateral or contralateral side to the axon. The response of each statocyst-driven descending interneuron to statocyst stimulation was differently modulated by leg movements in different conditions. During active leg movements, six statocyst-driven descending interneurons were activated regardless of whether a substrate was provided or not. In other two statocyst-driven descending interneurons, the excitatory input during leg movements was stronger when a substrate was provided than when it was not. One statocyst-driven descending interneuron received an excitatory input only during leg movements on a substrate, whereas another statocyst-driven descending interneuron did not receive any input during leg movements both on a substrate and in the air. These results suggest that the descending statocyst pathways are organized in parallel, each cell affected differently by behavioral conditions.Abbreviations EMG electromyogram - NGI nonspiking giant interneuron - SDI statocyst-driven descending interneuron     

Intracellular recordings from nonspiking interneurons in a semiintact,tethered walking insect

Nonspiking interneurons were investigated in a tethered, walking insect, Carausius morosus, that was able to freely perform walking movements. Experiments were carried out with animals walking on a lightweight, double-wheel treadmill. Although the animal was opened dorsally, the walking system was left intact. Intracellular recordings were obtained from the dorsal posterior neuropil of the mesothoracic ganglion. Nonspiking inter-neurons, in which modulations of the membrane potential were correlated with the walking rhythm, were described physiologically and stained with Lucifer Yellow. Interneurons are demonstrated in which membrane potential oscillations mirror the leg position or show correlation with the motoneuronal activity of the protractor and retractor coxae muscles during walking. Other interneurons showed distinct hyperpolarizations at certain important trigger points in the step cycle, for example, at the extreme posterior position. Through electrical stimulation of single, nonspiking interneurons during walking, the motoneuronal activity in two antagonistic muscles—protractor and retractor coxae—could be reversed and even the movement of the ipsilateral leg could be influenced. The nonspiking interneurons described appear to be important premotor elements involved in walking. They receive, integrate, and process information from different leg proprioceptors and drive groups of leg motoneurons during walking.     

Octopamine effects mimick state-dependent changes in a proprioceptive feedback system

The modulatory actions of the biogenic amine octopamine on the femur tibia (FT) control loop in the stick insect Carausius morosus were examined. The response properties of the FT control loop were determined under open loop conditions. Mechanical stimulation of the femoral chordotonal organ (fCO) was the input and tibial movement and motoneuronal activity were measured as the output of the system. Following octopamine injection into the hemolymph of intact, inactive animals, two consecutive phases occurred at the behavioral level. Octopamine caused initially an activation of the animal. During this first phase (3.5–12 min duration) the response properties of the FT control loop were similar to those found in animals that were activated by tactile stimuli under normal conditions. Afterward, animals became inactive. During this second phase (15–20 min duration), the gain of the control loop was zero and no resistance reflex in the FT joint was generated in response to fCO stimulation. However, active movements of the tibia could still be elicited. As we could show in restrained animals, where dl-octopamine was applied topically onto the undesheated mesothoracic ganglion, the complete suppression of the resistance reflex on the motoneuronal level was dose dependent starting at concentrations of 5 ± 10^?3 M octopamine. We could show that octopamine specifically suppressed the pathways involved in the resistance reflex, while feedback loop responses to fCO stimuli typical for active animals could still be elicited. Our results indicate that an increase in the octopamine concentration mimicks activation of the animal: Properties being characteristic for the control of the FT joint in the inactive animal are inhibited by octopamine, while properties of the FT control loop typical for the active animal appear to be facilitated following octopamine injection. The results clearly demonstrate that different pathways in the neuronal network underlying the FT control loop are involved in the responses of the control loop to fCO stimuli in the inactive and active behavioral states of the stick insect. © 1993 John Wiley & Sons, Inc.     

Neural control of ventilation in the shore crab, Carcinus maenas. II. Frequency-modulating interneurons

1. We have identified a class of nonspiking interneurons which can control the frequency of ventilation in a graded manner. These frequency modulating interneurons (FMis) also receive synaptic inputs in-phase with the ventilatory motor output providing a functional positive feedback loop in the ventilatory system. The class of FMis is composed of three morphologically and physiologically distinct interneurons, FMi1, FMi2 and FMi3. 2. Depolarization of FMi1 increases the rate of ventilation, while hyperpolarization decreases the rate (Fig. 1). This control is restricted to a single ventilatory central pattern generator (CPG), (Fig. 2), although FMi1 sends processes into the neuropils of both hemiganglionic CPGs (Fig. 3). 3. Hyperpolarization of FMi2 increases the rate of both ventilatory CPGs while depolarization of this cell slows and eventually arrests the rhythm (Figs. 5 and 6). FMi2 receives a synaptic input correlated with the motor output of each of the ventilatory CPGs (Fig. 4). During periods of reversed ventilation, this cell is abruptly hyperpolarized and continues to be driven in-phase with the ventilatory motor output (Fig. 7). 4. Hyperpolarization of FMi3 increases the rate of ventilation and depolarization decreases the rate of ventilation produced by both CPGs (Fig. 10). This control of the ventilatory rate by FMi3 is graded (Fig. 11). There is no apparent change in the membrane potential of FMi3 during reversed ventilation and it is morphologically distinct from FMi2. 5. FMi2 and FMi3 may be involved in the switch in ventilatory motor pattern from forward to reversed ventilation. Hyperpolarization of FMi2 and depolarization of FMi3 can elicit bouts of reversed ventilation from both CPGs (Fig. 13). 6. These results suggest that the FM interneurons act in parallel to control the frequency of ventilation and may act as integrating elements between spiking 'command' fibers in the circumesophageal connectives and the nonspiking interneurons of the ventilatory CPG.     

GABAergic and glutamatergic inhibition of nonspiking local interneurons in the terminal abdominal ganglion of the crayfish

Nonspiking local interneurons in the terminal abdominal ganglion of the crayfish Procambarus clarkii receive inhibitory inputs from mainly glutamatergic spiking local interneurons and GABAergic nonspiking interneurons. In this study, the inhibitory responses of nonspiking interneurons to local application of glutamate and GABA into the neuropil were compared. Glutamate and GABA injection mediated the hyperpolarization of the nonspiking interneurons with an increase in membrane conductance. The glutamate-mediated membrane hyperpolarization was reversed by injection of 1 or 2 nA hyperpolarizing current. By contrast, more than 3 nA hyperpolarizing current was frequently necessary to reverse the GABA-mediated hyperpolarization. Bath application of a chloride channel blocker, 50 microM picrotoxin (PTX), reduced the glutamate-mediated hyperpolarization, but had no effect on the GABA-mediated hyperpolarization. The GABA-mediated hyperpolarization was not consistently affected by bath application of low chloride solution. These results suggest that the glutamate-mediated inhibition was related to the gating of a Cl(-) conductance, while the GABA-mediated inhibition was not. Electrical stimulation of sensory afferents innervating the exopodite elicited ipsps in uropod opener motor neurons. These sensory-evoked ipsps were also PTX-insensitive, suggesting GABAergic nonspiking interneurons could be the predominant premotor elements in organizing the uropod motor control system.