Elevator Motoneurons Research Articles

Postembryonic development of centrally generated flight motor patterns in the hawkmoth, Manduca sexta

This study analyses the maturation of centrally generated flight motor patterns during metamorphosis of Manduca sexta. Bath application of the octopamine agonist chlordimeform to the isolated central nervous system of adult moths reliably induces fictive flight patterns in wing depressor and elevator motoneurons. Pattern maturation is investigated by chlordimeform application at different developmental stages. Chlordimeform also induces motor patterns in larval ganglia, which differ from fictive flight, indicating that in larvae and adults, octopamine affects different networks. First changes in motoneuron activity occur at the pupal stage P10. Rhythmic motor output is induced in depressor, but not in elevator motoneurons at P12. Adult-like fictive flight activity in motoneurons is observed at P16 and increases in speed and precision until emergence 2 days later. Pharmacological block of chloride channels with picrotoxin also induces fictive flight in adults, suggesting that the pattern-generating network can be activated by the removal of inhibition, and that proper network function does not rely on GABA(A) receptors. Our results suggest that the flight pattern-generating network becomes gradually established between P12 and P16, and is further refined until adulthood. These findings are discussed in the context of known physiological and structural CNS development during Manduca metamorphosis.

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.

Reflex activation of locust flight motoneurones by proprioceptors responsive to muscle contractions

This report investigates the reflex activation of locust flight motoneurones following their spiking activity. As shown elsewhere, an electrical stimulus applied to a flight muscle produces multiple waves of delayed excitation in wing elevator and depressor motoneurones. Nerve ablation experiments show that this response is initiated by the mechanical movement of the stimulated muscle, and not the antidromic spike evoked in the motoneurone. The delayed excitation still occurs in the absence of inputs from the wing receptor systems, and also when all other sources of afferent feedback are abolished, excepting thoracic nerve 2. Following complete deafferentation, spikes in flight motoneurones had no influence on other flight motoneurones. Numerous afferents in the purely sensory nerve 2 are excited by flight muscle contractions. The responses are consistent for repeated contractions of the same muscle, but differ when other muscles are stimulated. During tethered flight, changes in the activation of single flight muscles are reflected in changes of the nerve 2 discharge pattern. Electrical stimulation of this nerve causes delayed excitation of flight motoneurones, and can initiate flight activity. It is suggested that internal proprioceptors, such as those associated with nerve 2, will contribute to shaping the final motor output for flight behaviour.

Effects of afferent firing frequency on the amplitude of the monosynaptic EPSP elicited by trigeminal spindle afferents on trigeminal motoneurones

We have examined the effect of changes in afferent firing frequency on the monosynaptic EPSP elicited by trigeminal muscle spindle afferents in elevator motoneurones, using both paired pulse and repetitive activation of the masseter nerve. Both modes of stimulation resulted in significant facilitation of EPSP amplitude over intervals of 5–19 ms, but no significant change in EPSP amplitude at either longer or shorter intervals. The facilitation obtained stands in contrast to the predominant depression of EPSP amplitude reported in hindlimb motoneurones following stimulation at decreasing intervals.

Alteration of bursting properties in interneurons during locust flight.

1. The contribution of bursting properties to the generation of the flight motor pattern was examined for two identified interneurons (interneurons 566 and 567) in the flight system of the locust Locusta migratoria by means of intracellular recording and stimulation techniques. These interneurons are important elements in transmitting proprioceptive information from the hindwing tegula to wing elevator motoneurons. 2. Offset currents injected into these neurons revealed that bursts are triggered in the intact flying animal by synaptic input from tegula afferents (n = 10). These bursts lead to an amplification of proprioceptive input that is crucial for the generation of the intact flight motor pattern. In the absence of afferent input the activity of these neurons remained subthreshold for triggering a burst. This explains why these neurons exhibit only weak rhythmic oscillations in deafferented animals. 3. The property of interneuron 566 to burst was conditional, always being expressed during flight (n = 14) and occurring only occasionally in the quiescent animal. In the absence of flight, stimulation of tegula afferents never evoked bursts in interneuron 566 (n = 7) and depolarizing current pulses evoked weak bursts in only three of nine preparations. In 2 of 14 animals, bursting property of interneuron 566 was enhanced just after the termination of flight. 4. Variability in the bursting property was also found for interneuron 567. In the quiescent animal, tegula-evoked compound excitatory postsynaptic potentials were not sufficient to trigger bursts (n = 3) but depolarizing current pulses evoked always weak rhythmic bursting activity (n = 4). This bursting property was also variable and in one animal we found long-lasting plateau potentials that could be evoked by current injection after flight was elicited several times. 5. The data presented demonstrate that the capacity to burst is conditional in the interneurons 566 and 567. Bursting properties are always induced during flight and function to amplify proprioceptive pathways that are important for the generation of the intact flight motor pattern.

Monosynaptic EPSPs elicited by single interneurones and spindle afferents in trigeminal motoneurones of anaesthetized rats.

1. Our aim has been to quantify the monosynaptic connections of trigeminal interneurones and spindle afferents onto jaw-elevator motoneurones as a step towards identifying common features in organization of monosynaptic inputs onto motoneurones. We have used the intracellular variant of the spike-triggered averaging method to examine the connections of single identified trigeminal interneurones and jaw-elevator muscle spindle afferents onto single jaw-elevator motoneurones. The interneurones examined lay in the region immediately caudal to the trigeminal motor nucleus. The experiments were performed on rats anaesthetized with pentobarbitone, paralysed and artificially ventilated. 2. Ten EPSPs and eight IPSPs were obtained from examining the connections of seventeen interneurones to thirty-six motoneurones, suggesting a functional connectivity of 50% for individual interneurones onto elevator motoneurones. Fourteen EPSPs were obtained from examining the connections of thirteen spindle afferents onto twenty-seven motoneurones, giving a functional connectivity of 52% for individual spindle afferents onto elevator motoneurones. The amplitudes of the EPSPs elicited by interneurones ranged from 7-48 microV (mean = 17, S.D. = 12.5, n = 10) and from 7 to 289 microV (mean = 64, S.D. = 76.0, n = 14) for the spindle-mediated EPSPs; the difference in the two means was not significant (P = 0.07). 3. However, the amplitude of averaged responses obtained by signal averaging methods are dependent on the assumption that the postsynaptic response occurs following every impulse in the presynaptic neurone. We therefore estimated the percentage of sweeps which contained EPSPs triggered by the presynaptic neurone under study. In essence the method used consisted of visual inspection of the individual sweeps comprising an average in order to assess the occurrence of EPSPs within six separate time windows, each of duration +/- 0.3 ms. Five windows were placed at randomly selected times on average and were used to provide an estimate of the frequency of occurrence of randomly triggered EPSPs. The sixth window was centred on the start of the averaged EPSP and the frequency of occurrence of randomly triggered EPSPs was subtracted from the frequency of occurrence of EPSPs in this window to produce an estimate of the incidence of EPSPs triggered by the presynaptic neurone under study. 4. Values of the incidence of occurrence of EPSPs triggered by the presynaptic neurones ranged from 4.3 to 92% for the fifteen averaged EPSPs which could be analysed in this manner (two elicited by interneurones and thirteen by spindle afferents).(ABSTRACT TRUNCATED AT 400 WORDS)

Connections of the forewing tegulae in the locust flight system and their modification following partial deafferentation.

The flight motor pattern of the adult locust (Locusta migratoria L.) is able to recover from the loss of the hindwing tegulae. This recovery is due to a functional substitution of the hindwing tegulae by the forewing tegulae (Büschges, Ramirez, and Pearson, 1992). To assess changes in the pathways from the forewing tegulae in the flight system, we investigated the pathways of the forewing tegula in intact locusts and in animals 2 weeks after hindwing tegula removal. The following physiological alterations in these pathways were found to be associated with the recovery: (1) In the intact locusts, the connections of forewing tegula afferents to flight interneurons are variable but this variability did not occur in recovered animals, and (2) larger numbers of forewing tegula afferents connect to interneurons that excite elevator motoneurons (interneurons 566 and 567) and to an interneuron that inhibits depressor motoneurons (interneuron 511). The size of unitary excitatory postsynaptic potentials (EPSPs) evoked by signal forewing tegula afferents was found not to be altered in recovered animals. The changes in connectivity of forewing tegula afferents are correlated with morphological alterations in the structure of the terminal processes of the afferents and with sprouting of some branches of interneurons receiving input from these afferents.

Octopaminergic modulation of interneurons in the flight system of the locust

1. Modulatory effects of octopamine perfusion on identified central neurons in the flight system of the locust Locusta migratoria were examined by means of intracellular recordings from the isolated metathoracic ganglion. 2. Octopamine increased the excitatory response of elevator motoneurons to electrical stimulation of the hindwing tegula and increased the probability of triggering rhythmic activity in the flight system by current injection into single interneurons. 3. These effects of octopamine on the flight system are due in part to octopamine inducing intrinsic bursting properties in flight interneurons. Plateau potentials were evoked in these interneurons by synaptic input from tegula or by the injection of depolarizing current pulses. These potentials were prematurely terminated by hyperpolarizing currents, and their generation was voltage sensitive in that they were suppressed with hyperpolarizing offset currents. 4. Longer depolarizing current pulses evoked endogenous bursting in a number of flight interneurons. This rhythmic bursting was reset by the injection of pulses of hyperpolarizing currents. The frequency of bursting was dependent on the injected current strength. 5. The injection of hyperpolarizing current into flight interneurons during octopamine-induced rhythmic activity lead to sudden decreases in the amplitude of the depolarizations thus indicating that plateau potentials contribute to the generation of the rhythmic depolarizations. 6. The shape of the depolarizations, the duration of the bursts (50-75 ms), and the frequency range of endogenous bursting (4-16 Hz) as seen in individual interneurons during octopamine perfusion were similar to the corresponding characteristics in the same neurons during wind-induced flight activity in deafferented locusts. This correspondence suggests that intrinsic bursting properties may play an important role in generating the normal motor pattern for flight.

Adaptive Modifications in the Flight System of the Locust After the Removal Of Wing Proprioceptors

ABSTRACT Previous investigations on the flight system of the locust have found that removal of the wing tegulae in mature locusts (Locusta migratoria) results in an immediate change in the flight motor pattern: the wingbeat frequency (WBF) decreases, the interval between the activity of the depressor and the elevator muscles (the D-E interval) increases, and the phase of the elevator activity in the depressor cycle increases. Here we report the results of a detailed quantitative analysis of these changes. We also examined the flight motor pattern for up to 14 days after removal of the tegulae and found that the changes caused by this operation were not permanent. Beginning on the first day after the operation there was a time-dependent recovery of the WBF, the D-E interval and the phase towards their normal values. In about 80% of the experimental animals the flight motor pattern recovered almost completely. Intracellular recordings from elevator motoneurones showed that this recovery was associated with changes in the pattern of excitatory input to these motoneurones. The modification of activity in elevator motoneurones was dependent on afferent input since complete deafferentation of recovered animals resulted in a motor pattern similar to that following deafferentation of normal animals.

Chemical deafferentation of the locust flight system by phentolamine

1. Phentolamine was injected into the haemolymph of locusts, Locusta migratoria, and its effects on the flight system were analyzed using electrophysiological techniques. 2. Doses of 150 microliters at 10(-2) M phentolamine inactivated the wing stretch-receptors and tegulae without influencing the central nervous system (CNS). The lack of effect on the CNS was demonstrated by the absence of any effect on the flight motor pattern in animals that had been mechanically deafferented prior to the administration of phentolamine. From these observations we conclude that phentolamine can be used to chemically deafferent the flight system of the locust. Consistent with this conclusion is that the administration of phentolamine in intact animals changed the flight motor pattern so that it resembled the pattern occurring in mechanically deafferented animals. 3. The two main advantages of deafferenting the flight system by injecting phentolamine were a) intracellular recordings from central neurons could be easily maintained during the process of deafferentation, and b) the contribution of different groups of proprioceptors to the generation of the motor pattern could be assessed since not all proprioceptors were inactivated simultaneously. 4. By intracellularly recording from elevator motoneurons and administering phentolamine we confirmed a number of previous results related to the function of the wing stretch-receptors and the tegulae.

Influence of input from the Forewing Stretch Receptors on Motoneurones in Flying Locusts

ABSTRACT Previous studies on the forewing stretch receptors (FSRs) of locusts have suggested that feedback from these receptors during flight contributes to the excitation of depressor motoneurones and reduces the duration of depolarizations in elevator motoneurones. We have investigated these proposals by measuring the timing of FSR activity relative to depressor activity and by examining the effects of stimulating the FSRs on the membrane potential oscillations in flight motoneurones. Activity in the FSRs was recorded in tethered intact animals flying in a windstream and in preparations that allowed intracellular recordings from motoneurones during flight activity. The timing of FSR activity was similar in both preparations. In most animals we observed that at normal wingbeat frequencies (about 20 Hz) the activity in the FSRs commenced after the onset of activity in the wing depressor muscles. As wingbeat frequency declined there was a progressive advance of FSR activity relative to depressor activity. Most of the spikes in each burst of FSR activity occurred during the time that the membrane potential in depressor motoneurones was repolarizing. Electrical stimulation of the FSRs timed to follow the onset of depressor activity slowed the rate of repolarization, decreased the peak hyperpolarization and increased the rate of the following depolarization in depressor motoneurones. In elevator motoneurones, the same pattern of FSR stimulation produced an additional excitatory input during the depolarization phase and, at low wingbeat frequencies, reduced the duration of the peak depolarizations. The reduction in the duration of the peak depolarization in elevator motoneurones was not strongly correlated to the reduction in cycle period. We propose that the primary reason why input from the FSRs increases wingbeat frequency is because this input reduces the degree of hyperpolarization in depressor neurones and thus promotes an earlier onset of the next depolarization in these neurones.

Contrasting effects of urethane and pentobarbitone anaesthesia on the electrical properties of rat jaw-elevator motoneurones

Our main finding is that elevator motoneurones do not show sustained firing to intracellular injections of depolarising current pulses in rats anaesthetised with urethane. In contrast, virtually all elevator motoneurones show sustained firing in pentobarbitone-anaesthetised rats. The differences in firing are not associated with significant differences in membrane potential, spike amplitudes, AHP amplitude or duration, input resistance, time constant or rheobase ( P > 0.06 in all cases). However, there are clear differences in the extent of sag seen under the two anaesthetics and so we tentatively suggest that the anaesthetics may differ in their effects on the inward rectifier.

The membrane properties and firing characteristics of rat jaw‐elevator motoneurones.

1. We have determined the membrane and firing properties of fifty-six jaw-elevator motoneurones in rats that were anaesthetized with pentobarbitone, paralysed and artificially ventilated. 2. Forty-two neurones were identified as masseter motoneurones and fourteen as masseter synergist motoneurones. The membrane potentials for the sample ranged from -60 to -86 (mean = -68; S.D. = 7.3; n = 56), and spike amplitudes from 50 to 95 mV. The duration of the after-hyperpolarization following antidromic spikes in masseter motoneurones ranged from 15 to 50 ms (mean = 30; S.D. = 12.8) and their amplitudes from 1.0 to 4.5 mV (mean = 2.7; S.D. = 2.2; n = 42). 3. The mean input resistance for the total sample was 2.3 M omega (S.D. = 0.9; n = 56), membrane time constant 3.9 ms (S.D. = 0.9; n = 48) and rheobase 4.2 nA (S.D. = 2.6; n = 56). The distribution of these parameters was independent of membrane potential. We found no significant interrelationships between the membrane properties and one interpretation of this is that our sample may be drawn from a homogenous population of motoneurones. We also suggest that elevator motoneurones may have a lower Rm (specific membrane resistivity) value than cat hindlimb motoneurones because they have a similar range of input resistance values but only half the total surface area. 4. Forty-six out of forty-nine neurones fired repetitively to a depolarizing current pulse at a mean threshold of 1.6 x rheobase. Current-frequency plots were constructed for thirteen neurones and all but one showed a primary and secondary range in the firing of the first interspike interval. The mean slope in the primary range was 31 impulses s-1 nA-1 and 77 impulses s-1 nA-1 for the secondary range. The mean minimal firing frequency for steady firing was 26 impulses s-1 and, in response to an increase of stimulation, the rate increased monotonically with a slope of 11 impulses s-1 nA-1. 5. The dynamic sensitivity of twelve neurones was assessed from their response to ramp waveforms of current of constant amplitude but varying frequencies (0.2-2 Hz). Firing initially increased along a steep slope up to a frequency of between 40 and 60 impulses s-1 and then increased along a much shallower slope. Both the threshold for eliciting firing and the firing at the transition point of the two slopes remained constant with changes in ramp frequency.(ABSTRACT TRUNCATED AT 400 WORDS)

The monosynaptic excitatory connections of single trigeminal interneurones to the V motor nucleus of the rat.

1. We have used the extracellular spike-triggered averaging method to identify a population of trigeminal interneurones that make monosynaptic connections within the V motor nucleus. The experiments were performed on rats anaesthetized with pentobarbitone (60 mg/kg I.V.; supplementary doses given as necessary to maintain a deep level of anaesthesia). 2. A tungsten microelectrode (tip exposure of some 200 microns) was inserted into the masseter motoneurone pool to allow recording of extracellular activity. A glass electrode filled with DL-homocysteic acid was used to make simultaneous extracellular recordings of the firing of single neurones in the region immediately caudal to the motor nucleus. 3. Fifty-eight out of 166 interneurones tested gave unitary extracellular fields in the motor nucleus. The responses consisted of a terminal spike (presynaptic spike) followed by a negative field of duration approximately 3 ms and amplitude 0.4-10.8 microV. The mean latency between the positive peak of the terminal spike and the onset of the field (synaptic delay) was 0.43 ms (S.D. = 0.10 ms), and the mean latency from the onset of the interneurone spike to the positive peak of the presynaptic spike was 0.35 ms (S.D. = 0.22 ms). Thus the interneurones project directly to the motor nucleus where they then make monosynaptic connections. 4. The negative extracellular fields were taken to reflect an excitatory synaptic input onto neurones within the motor nucleus. The fields were of maximum amplitude at the point of maximum masseter motoneurone antidromic field, suggesting that the connection may be onto elevator motoneurones. 5. The location of the interneurone appeared to the main factor governing the likelihood of obtaining a field. Interneurones located more than 400 microns from the caudal border of the motor nucleus rarely produced fields whereas most of those located within this distance gave fields. This pattern of distribution is strikingly similar to that of trigeminal interneurones labelled by the transneuronal transport of wheatgerm agglutinin-horseradish peroxidase after an intramuscular injection of the tracer into the masseter muscle. We suggest that this provides electrophysiological support for the suggestion that the tracer does indeed label interneurones by means of retrograde transsynaptic transport.

Excitatory pathways from Forel's field H to head elevator motoneurones in the cat

Projections of neurones in Forel's field H (FFH) to the upper cervical cord and to the lower brainstem were demonstrated by retrograde labelling of the neurones with horseradish peroxidase (HRP). Systematic threshold mapping for evoking antidromic spikes of FFH neurones revealed that they projected to the neck motor nuclei and to pontomedullary reticular formation (PMRF). Stimulation of FFH evoked large monosynaptic excitatory postsynaptic potentials (EPSPs) in reticulospinal neurones (RSNs) of the PMRF, and mono- and disynaptic EPSPs in the dorsal neck motoneurones. Above EPSPs were evoked from areas confined to FFH, thus indicating that they were elicited by stimulation of FFH neurones. Monosynaptic EPSPs in motoneurones were small but disynaptic EPSPs were markedly facilitated following stimulation with train pulses, becoming several times larger than the monosynaptic EPSPs. Disynaptic EPSPs were supposed to be relayed by RSNs in the PMRF which are known to project to dorsal neck motoneurones. The mono- and disynaptic EPSPs were induced chiefly in motoneurones of the head elevator (m. biventer cervicis and complexus) and rarely of the neck lateral flexor (m. splenius). It was suggested that FFH neurones are involved in the control of vertical head movements.

Connections of Hindwing Tegulae with Flight Neurones in the Locust, Locusta Migratoria

ABSTRACT The connections of afferents from the hindwing tegulae to flight motoneurones and interneurones in the locust, Locusta migratoria, have been determined by selectively stimulating the tegula afferents while recording intracellularly from identified neurones in the meso- and metathoracic ganglia. Electrical stimulation of the hindwing tegula nerve (nerve ICla) revealed two groups of afferents distinguished by a difference in their conduction velocities. Both groups of afferents made excitatory connections to hindwing elevator motoneurones in the ipsilateral half of the metathoracic ganglion. Latency measurements indicated that these connections were monosynaptic. Stimulation of the hindwing tegula nerve also evoked excitatory postsynaptic potentials (EPSPs) in elevator motoneurones in the mesothoracic ganglion and in the contralateral half of the metathoracic ganglion, and inhibitory postsynaptic potentials (IPSPs) in forewing and hindwing depressor motoneurones. The latencies of these evoked EPSPs and IPSPs indicated that the initial responses were produced via interneuronal pathways. None of the recordings revealed EPSPs in depressor motoneurones or IPSPs in elevator motoneurones in response to hindwing tegula stimulation. This observation differs from that in Schistocerca gregaria where it has been reported that the large tegula afferents produce EPSPs in depressors and IPSPs in elevators (Kien & Altman, 1979). Some of the interneurones in disynaptic excitatory and inhibitory pathways to motoneurones were identified. These interneurones received input from both hindwing tegulae and were readily excited beyond threshold by mechanical stimulation of the tegulae or by electrical stimulation of the tegula afferents. The contribution of one excitatory interneurone to the electrically evoked EPSPs was assessed by blocking spike initiation in the interneurone while recording simultaneously from a flight motoneurone. Based on our observations of the central connections of tegula afferents to flight motoneurones and the previously reported discharge patterns of these afferents during tethered flight (Neumann, 1985), we propose that a major function of the hindwing tegulae in L. migratoria is to generate the initial depolarizations in forewing and hindwing elevator motoneurones during flight. Consistent with this proposal was our finding that ablation of the hindwing tegulae delayed the onset of elevator activity relative to the onset of the preceding depressor activity.

Intracellular recordings from interneurons and motoneurons in intact flying locusts

A preparation is described in which it is possible to record intracellularly from identified motoneurons and interneurons during flight in intact tethered locusts. Intracellular recordings could be obtained from either the large somata of the motoneurons or from the neuropil processes of interneurons and motoneurons in either the meso- or metathoracic ganglion. Intracellular recordings from motoneuron somata were sufficiently stable to allow surgical manipulations, e.g. deafferentation, of the nervous system without the loss of penetration. Recordings from neuropil processes required stabilizing the ganglion by sandwiching it between two supports. The preparation is suitable for the cellular analysis of many aspects of motor patterning in the flight system of the locust. So far we have used it to make a direct comparison between the patterns of synaptic activity in intact and deafferented animals. This comparison shows that sensory feedback from wing proprioceptors strongly influences the activity in elevator motoneurons and flight interneurons. From these and other observations we conclude that proprioceptive feedback is essential for generating important features of the intact motor pattern and that wing receptors are integral elements of the intact flight pattern generator.

Coupling of flight initiation to the jump in locusts

1. In adult locusts' wing opening for flight occurs soon after a jump is triggered. Previous studies have shown that the interval between the triggering of a jump and the initial wing movement (or the start of elevator muscle activity) is often too short for either the loss of tarsal contact with the ground or the self-generated air stream on the head to be responsible for the onset of wing opening. Thus it has been postulated that the system generating the motor program for the jump is directly linked to the system generating flight motor activity. To investigate this proposal we have recorded activity in flight motoneurons and interneurons during bilateral kicks of the hindlegs. 2. The preparation was arranged to allow intracellular recording from flight motoneurons and interneurons during hindleg kicks. Kicks were readily evoked by mechanical stimulation of the abdomen, and the motor activity associated with the kicks was similar to that for a jump in unrestrained animals. 3. Short sequences of flight activity were often associated with hindleg kicks. The time of onset of flight activity relative to the time kicks were triggered was variable, and often flight activity commencedbefore the kicks were triggered. The probability of flight activity being initiated increased throughout the co-contraction phase with the peak probability being close to the time kicks were triggered. Thus it appears that the flight system receives a progressively increasing excitatory input during the co-contraction phase of the kick, and that the onset of flight activity isnot tightly linked to the system triggering the kick. 4. Intracellular recordings from flight motoneurons showed that wing elevator motoneurons often received an excitatory input during the co-contraction phase, whereas wing depressor motoneurons either showed no change in membrane potential or were slightly hyperpolarized during co-contraction. These recordings failed to reveal any significant input to flight motoneurons at the time a kick was triggered. 5. The lack of any influence of the trigger system on the flight system was also apparent in recordings from identified flight interneurons. None consistently showed a synaptic response timelocked to triggering but many received synaptic input during the co-contraction phase. Those receiving excitatory input were also those excited by wind on the head, while those receiving inhibitory input were hyperpolarized by wind on the head. 6. We conclude that the flight system receives an excitatory input during the co-contraction phase of the kick, and that this input produces many of the same changes in membrane potential in interneurons and motoneurons as does a wind stream to the head (a stimulus known to readily evoke flight activity). None of our data indicates that the system triggering the kick is responsible for exciting the flight system. We propose that in an intact animal the initiation of flight activity following a jump is facilitated by an excitatory input to the flight system during the co-contraction phase of the jump. The origin of this input has not been determined.

Integration of nonphaselocked exteroceptive information in the control of rhythmic flight in the locust.

The integration of exteroceptive information in the flight control system of the locust was studied by determining the cellular basis of ocellar- (simple eye) mediated control of flight. Neural interactions that transform phase-independent sensory input into phase-specific motor output were characterized. Ocellar information about course deviations during flight was conveyed to the segmental thoracic ganglia by three pairs of large fast multimodal descending neurons. These made connections with thoracic motoneurons directly, via short-latency mono-or disynaptic pathways, and indirectly, via a population of intercalated thoracic interneurons. The synaptic potentials caused in the motoneurons by the direct pathway occurred at short latency and were adequate for summation with other types of sensory input. However, the strength of the synaptic effects of this pathway was weak compared with the central flight oscillator drive to the same motoneurons. In contrast, synaptic potentials evoked by the descending neurons in the thoracic interneurons were often large and brought these cells close to threshold. In turn, these interneurons always had stronger synaptic effects on postsynaptic flight motoneurons than did the descending neurons alone. We conclude that the indirect interneuronal pathway is more powerful in its effects on motoneurons than the direct pathway. Premotor thoracic interneurons, which received ocellar input appropriate for a role in correctional steering, were also rhythmically modulated during flight motor activity in phase with either depressor or elevator motoneurons. This phasic modulatory drive occurred in deafferented preparations, indicating that its source is the central oscillator for flight. Presentation of ocellar stimulation during flight motor activity showed that the central oscillatory modulation of the thoracic interneurons gated the transmission of sensory information through these interneurons. Ocellar-mediated postsynaptic potentials influenced the firing of thoracic interneurons only if they arrived during the proper phase of rhythmic drive. Thus the transmission of ocellar information from interneuron to motor neuron is possible only during appropriate phases of the flight cycle.

Patterns of synaptic input to identified flight motoneurons in the locust

1. We examined the pattern of synaptic input to identified flight motoneurons of the locust,Locusta migratoria. The preparation we used was one in which rhythmic motor activity resembling flight activity could be generated following removal of all sensory input from wing receptors. Intracellular recordings were made from the main neuropil processes of all the 17 different types of fast motoneurons in the meso- and metathoracic ganglia which innervate the main flight muscles. Motoneurons were identified anatomically by intracellular staining with Lucifer yellow following recording. 2. The pattern of synaptic input was similar in all elevator motoneurons (4 different types in each of the two ganglia). Three distinct components were observed in the profile of synaptic activity in these motoneurons. The first was a relatively slow depolarization beginning immediately after the end of a depolarization in depressor motoneurons, the second was a rapid depolarization which began at a variable interval after the beginning of the initial slow depolarization, and the third was a rapid repolarization occurring in-phase with depressor depolarizations. The similarity of synaptic input to elevator motoneurons prevented the use of physiological criteria for the identification of individual elevator motoneurons. 3. Unlike the elevators, the depressor motoneurons do not form a homogeneous group with regard to the pattern of centrally derived synaptic input. Different patterns of input were observed in different depressor motoneurons, including differences in input to homologous motoneurons in the meso- and metathoracic ganglia. The most obvious difference between the profiles of synaptic input to elevator and depressor motoneurons was that the depolarizations in the latter consisted of only a single component, the duration of which increased relatively slowly with increases in cycle time. Knowledge of the recording site within a ganglion and the pattern of synaptic input allowed depressor motoneurons to be identified individually. 4. Simultaneous recordings from an elevator and a depressor motoneuron within the same ganglion showed that the synaptic input to the two groups of motoneurons is not symmetrically timed. Each depolarization in depressor motoneurons began immediately following the end of a rapid depolarization in elevators, but the beginning of the rapid depolarizations in elevators was delayed following the end of each depressor depolarization by an amount depending on cycle time. A single depressor depolarization never occurred in the absence of a preceding rapid elevator depolarization. We conclude that the basic unit of activity in the central oscillator is an elevator followed by a depressor depolarization sequence. 5. Simultaneous recordings from homologous motoneurons in the meso- and metathoracic ganglia of deafferented preparations revealed that the depolarizations in elevator motoneurons in the two ganglia were in-phase. In depressors, however, the depolarizations in hindwing motoneurons led those in homologous forewing motoneurons by 5 to 15 ms indicating that central processes are partly, but not completely, responsible for establishing the relative timing of fore and hind wing movements in normal flight. This basic difference in the intersegmental driving of elevator and depressor motoneurons in deafferented preparations was confirmed in electromyographic recordings from homologous fore- and hindwing muscles.