Recovery of the flight system following ablation of the tegulae in immature adult locusts

1996 ◽  
Vol 199 (6) ◽  
pp. 1395-1403 ◽  
Author(s):  
C Gee ◽  
R Robertson
Keyword(s):  
Locusta Migratoria ◽  
Motor Pattern ◽  
Recovery Period ◽  
Wingbeat Frequency ◽  
Mature Adult ◽  
Flight System ◽  
Mature Adults ◽  
Locust Flight ◽  
Adult Locust ◽  
The Individual

The capacity of the flight system to recover from ablation of the tegulae was studied in immature adult Locusta migratoria and compared with recovery in mature adults. We ablated the hindwing tegulae or all tegulae in adult locusts either 1 day after the imaginal moult (immature locusts) or 2 weeks after the imaginal moult (mature locusts). We monitored recovery throughout the recovery period by using a stroboscope to measure the wingbeat frequency of tethered locusts. In addition, we measured other parameters of the flight motor pattern using electromyographic electrodes implanted into recovered locusts. Both methods of monitoring recovery yielded the same results. There was no reduction, during adult maturation, in the capacity of the locust flight system to recover from the loss of these proprioceptors. Plasticity of the locust flight system was therefore maintained in the mature adult locust. This suggests that the flight system is not fixed and simply implemented when the locust reaches adulthood, but that the circuitry can be remodelled throughout the animal's life to produce behaviour adapted to the needs and constraints of the individual.

ADAPTIVE MODIFICATIONS IN THE FLIGHT SYSTEM OF THE LOCUST AFTER THE REMOVAL OF WING PROPRIOCEPTORS

1991 ◽  
Vol 157 (1) ◽  
pp. 313-333 ◽  
Author(s):  
ANSGAR BÜSCHGES ◽  
KEIR G. PEARSON
Keyword(s):  
Normal Values ◽  
Locusta Migratoria ◽  
Motor Pattern ◽  
Afferent Input ◽  
Excitatory Input ◽  
Time Dependent ◽  
Intracellular Recordings ◽  
Wingbeat Frequency ◽  
Flight System ◽  
Flight Motor

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.

Plasticity of Synaptic Connections in Sensory-Motor Pathways of the Adult Locust Flight System

1997 ◽  
Vol 78 (3) ◽  
pp. 1276-1284 ◽  
Author(s):  
Harald Wolf ◽  
Ansgar Büschges
Keyword(s):  
Electric Stimulation ◽  
Motor Pattern ◽  
Competitive Interactions ◽  
Synaptic Connections ◽  
Flight System ◽  
Motor Pathways ◽  
Synaptic Contacts ◽  
Locust Flight ◽  
Sensory Motor ◽  
Adult Locust

Wolf, Harald and Ansgar Büschges. Plasticity of synaptic connections in sensory-motor pathways of the adult locust flight system. J. Neurophysiol. 78: 1276–1284, 1997. 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.

Neural circuits in the flight system of the locust

1985 ◽  
Vol 53 (1) ◽  
pp. 110-128 ◽  
Author(s):  
R. M. Robertson ◽  
K. G. Pearson
Keyword(s):  
Locusta Migratoria ◽  
Motor Pattern ◽  
Short Latency ◽  
Dependent Manner ◽  
Flight System ◽  
Neuronal Connections ◽  
Staining Techniques ◽  
Constant Duration ◽  
To Receive ◽  
Flight Motor

Circuitry in the flight system of the locust, Locusta migratoria, was investigated by use of intracellular recording and staining techniques. Neuronal connections were established by recording simultaneously from neuropile segments of pairs of identified interneurons. Brief depolarizing current pulses delivered to interneurons 301 and 501 reset the flight rhythm in a phase-dependent manner, thus establishing the importance of these neurons in rhythm generation. Interneuron 301 was found to make a strong delayed excitatory connection with 501 and to receive a short-latency inhibitory connection from 501. The circuit formed by 301 and 501 appears suited for promoting rhythmicity in the flight system. The delayed excitatory potential recorded in 501 following each spike of 301 was reversed by hyperpolarizing 501. This potential and short-latency inhibitory postsynaptic potentials from 301 to other interneurons were blocked with the application of picrotoxin. We conclude that the delayed excitation is produced via a disynaptic pathway from 301 to 501, with 301 inhibiting in a graded manner the tonic release of transmitter from one or more unidentified intercalated neurons. Interconnections between the 301-501 circuit and other identified interneurons were discovered. This circuitry can account for two features of the flight motor pattern recorded in deafferented preparations. These features are the constant-latency relationship between depolarizations in elevator and depressor motoneurons and the relatively constant duration of depressor motoneuron bursts. The locust flight system shares general features with other described rhythm-generating systems. These include the occurrence of graded interactions, the probability of multiple oscillatory mechanisms, and a predominance of inhibitory connections. Its uniqueness lies in the way that components and processes are assembled and operate.

Relationships between body mass, motor output and flight variables during free flight of juvenile and mature adult locusts, Schistocerca gregaria

2000 ◽  
Vol 203 (18) ◽  
pp. 2723-2735 ◽  
Author(s):  
H. Fischer ◽  
W. Kutsch
Keyword(s):  
Body Mass ◽  
Schistocerca Gregaria ◽  
Flight Speed ◽  
Free Flight ◽  
Wingbeat Frequency ◽  
Motor Patterns ◽  
Mature Adult ◽  
Body Angle ◽  
Flight System ◽  
Functional Relationships

Little information is available about how the adult locust flight system manages to match the aerodynamic demands that result from an increase in body mass during postmoult maturation. In Schistocerca gregaria of both sexes, flight variables, including flight speed, ascent angle and body angle, were investigated under closed-loop conditions (i.e. during free flight) as a function of adult maturation. Motor patterns were examined by telemetric electromyography in juvenile and adult mature animals of both sexes. Functional relationships between particular flight variables were investigated by additional loading of the animals and by reductions in wing area. The results indicate that an increase in flight speed as the flight system matures enables it to match the aerodynamic demands resulting from increases in body mass. Furthermore, the data suggest that this postmoult increase in flight speed is not simply a consequence of the increase in wingbeat frequency observed during maturation. The instantaneous body angle during flight is controlled mainly by aerodynamic output from the wings. In addition, the mean body angle decreases during maturation in both sexes, and this may play an important part in the directional control of the resultant flight force vector.

The forewing tegulae: their significance in steering manoeuvres and free flight in Locusta migratoria

1998 ◽  
Vol 76 (4) ◽  
pp. 660-667 ◽  
Author(s):  
Christine E Gee ◽  
Kelly L Shoemaker ◽  
R Meldrum Robertson
Keyword(s):  
Muscle Activation ◽  
Locusta Migratoria ◽  
Motor Pattern ◽  
Afferent Input ◽  
Open Loop ◽  
Free Flight ◽  
Flight System ◽  
Depressor Muscle ◽  
Flight Motor

The flight system of Locusta migratoria is widely used to investigate the principles of sensory-motor control. The four tegulae are proprioceptors of the flight system that are active during the downstroke and provide afferent input to flight-system neurons. While the role of the hindwing tegulae in the flight motor pattern has been well characterized, the role of the forewing tegulae is unclear. We tested whether the forewing tegulae may be more important for the generation of intentional steering manoeuvres than for generation of the basic flight motor pattern. Following ablation of the forewing tegulae, tethered flying locusts continued to generate characteristic intentional steering manoeuvres in open-loop conditions. In contrast, we found that locusts were less likely to sustain unrestrained free flight following ablation of the forewing tegulae. We also found that the number of spikes in a forewing depressor muscle increased, as did the hindwing to forewing delay in elevator-muscle activation after ablation of the forewing tegulae. We conclude that the forewing tegulae promote free flight in locusts and we discuss the role they may play in locust flight.

Postembryonic development of an insect sensory system: ingrowth of axons from hindwing sense organs in Locusta migratoria

1978 ◽  
Vol 202 (1149) ◽  
pp. 497-516 ◽  
Keyword(s):  
Locusta Migratoria ◽  
Sensory System ◽  
Postembryonic Development ◽  
Stretch Receptor ◽  
Sensory Nerves ◽  
Chordotonal Organ ◽  
Wingbeat Frequency ◽  
Adult Locust ◽  
Wing Bud ◽  
To Come

Axon counts have been made from electron micrographs of the hind­wing sensory nerves 1C 1 and 1D 2 in the adult locust and during develop­ment. In the adult, nerve 1C 1 contains approximately 1000 axons. At least a quarter have diameters over 1 µm, more than forty 5-12 µm. Seventy large axons come from the tegula, the rest from the wing. Nerve 1D 2 contains 400 axons, 64 between 1 µm and 6.5 µm in diameter. Large axons are assumed to come from the wing base chordotonal organ and stretch receptor, the remainder from thoracic hair fields. During development, axon numbers in nerve 1C 1 rapidly increase at the 4th instar, corresponding to the development of the wing bud. By the final moult there are over 2000 axons, half of which disappear in the two weeks after fledging. In nerve 1D 2 the stretch receptor and chor­dotonal axons are present from the first instar. Small fibres increase in number mainly in the 5th instar. In contrast to nerve 1C 1 there is no change in numbers after fledging. In both nerves, diameters and glial wrapping of axons increase in the two weeks after fledging, although the changes are more marked in nerve 1C 1 . The large input from the tegula suggests an important rôle in the phasic control of flight. The post-fledging increase in diameter and glial wrappings of tegula axons may influence the increase in wingbeat frequency with age.

scholarly journals Proprioceptive input patterns elevator activity in the locust flight system

1988 ◽  
Vol 59 (6) ◽  
pp. 1831-1853 ◽  
Author(s):  
H. Wolf ◽  
K. G. Pearson
Keyword(s):  
Motor Neuron ◽  
Hind Wing ◽  
Locusta Migratoria ◽  
Motor Pattern ◽  
Afferent Input ◽  
Neuron Activity ◽  
Late Component ◽  
Wingbeat Frequency ◽  
Stretch Receptors ◽  
Receptor Input

1. In the locust, Locusta migratoria, the roles of two groups of wing sense organs, hind wing tegulae and wing-hinge stretch receptors, in the generation of the flight motor pattern were investigated. A preparation was employed that allowed the intracellular recording of neural activity in almost intact tethered flying locusts or after selective manipulations of sensory input. The functions of the two sets of receptors were assessed 1) by studying the phases of their discharges in the wingbeat cycle (Fig. 3), 2) by the selective ablation of input from the receptors (Figs. 4-7), and 3) by the selective stimulation of the receptor afferents (Figs. 8-12). 2. Input from the tegulae was found to be responsible for the initiation of elevator activity (Figs. 9 and 10) and for the generation of a distinct initial rapid depolarization (Figs. 4, 5, and 8) characteristic of elevator motor neuron activity in intact locusts (Figs. 1 and 16). 3. Input from the wing-hinge stretch receptors was found to control the duration of elevator depolarizations by the graded suppression of a second late component of the elevator depolarizations as wingbeat frequency increased (Figs. 6, 7, 11, and 12). The characteristics of this late component of elevator activity suggested that it is generated by the same (central nervous) mechanism that produces the elevator depolarizations recorded in deafferented animals (Fig. 2). Apparently this late component contributes to the intact pattern of elevator depolarizations only at lower wingbeat frequencies and is abolished by the action of stretch-receptor input at frequencies above approximately 15 Hz (Figs. 1, 2, and 4). At these high wingbeat frequencies elevator activity is dominated by the rapid depolarizations generated as a result of tegula input. 4. The present study demonstrates 1) that the timing of elevator motor neuron activity is determined by phasic afferent input from tegulae and stretch receptors and 2) that input from the stretch receptors controls the duration of elevator activity in the wingbeat cycle following the wing movement that was responsible for the generation of the receptor discharge.

Tegula function during free locust flight in relation to motor pattern, flight speed and aerodynamic output

1999 ◽  
Vol 202 (6) ◽  
pp. 711-721 ◽  
Author(s):  
H. Fischer ◽  
E. Ebert
Keyword(s):  
Schistocerca Gregaria ◽  
Motor Pattern ◽  
Flight Speed ◽  
Adaptive Behaviour ◽  
Proprioceptive Information ◽  
Free Flight ◽  
Wingbeat Frequency ◽  
Motor Patterns ◽  
Flight System ◽  
Flight Parameters

Tegulae are complex proprioceptors at the wing base of locusts. Deafferentation of the tegulae causes a lack of specific phasic information related to the wing downstroke and the timing of the upstroke. Employing telemetry during free flight of the locust Schistocerca gregaria, we investigated the consequences of tegula ablation on free flight parameters including motor patterns (wingbeat frequency and the relationship between the activation of flight muscle antagonists), free flight speed and aerodynamic output. We investigated the role of the tegula pairs of both wings on the motor pattern generated in free-flying locusts. We show that the tegula organs are not essential for generating the motor patterns necessary for free flight. However, they are required for increasing the motor output to give additional effective lifting power during adaptive behaviour. We also investigated long-term changes in the free flight parameters after tegula ablation. The recovery of the adult flight system revealed in the present study suggests that there is adaptation to the loss of proprioceptive information; this argues for a full functional and behavioural recovery of the flight system of the locust under closed-loop conditions.

Octopaminergic modulation of interneurons in the flight system of the locust

1991 ◽  
Vol 66 (5) ◽  
pp. 1522-1537 ◽  
Author(s):  
J. M. Ramirez ◽  
K. G. Pearson
Keyword(s):  
Locusta Migratoria ◽  
Motor Pattern ◽  
Rhythmic Activity ◽  
Current Strength ◽  
Plateau Potentials ◽  
Excitatory Response ◽  
Flight System ◽  
Central Neurons ◽  
Current Pulses ◽  
Metathoracic Ganglion

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.

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