Flight Rhythm Research Articles

Determination of Hourly Distribution of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) Using Sex Pheromone and Ultraviolet Light Traps in Protected Tomato Crops

Tuta absoluta (Meyrick), a leafminer that damages tomato leaves, terminal buds, flowers, and fruits, is a destructive tomato pest and is responsible for 80–100% of tomato yield losses globally. Different insect species have different courtship responses and phototropic flight rhythms. Improving the trapping effects of the sex pheromone and light traps is important for constructing an IPM system for T. absoluta. The present study explored the hourly distribution of T. absoluta adults caught by the sex pheromone (on the ground) and UV light (380 nm) traps in greenhouses over 24 h. The responses of males to sex pheromone (false female) lures were detected at dawn and early morning. The responses lasted for 3 h, from 05:30 (1 h before sunrise) to 08:30 (2 h after sunrise), and 95.8% of the males were caught during this period. The peak of the male responses to the sex pheromone was detected at 07:30 (from 06:30 to 07:30, 1 h after sunrise), and 80.8% of the males were caught during this period. The flight of male (proportion of 54.3%) and female (45.7%) adults toward the UV light traps occurred from 19:30 (time of sunset) to 06:30 (time of sunrise), lasted for 11 h, and exhibited a scotophase rhythm; 97.4% of the adults were caught during this period. The peak of adults flying toward the UV light traps occurred at 21:30 (from 20:30 to 21:30, 2 h after sunset). The rhythms of males’ responses to the sex pheromone and of the adults’ flight toward the UV lights can help to reveal the mechanisms of chemotactic and phototactic responses and may play a significant role in constructing an IPM system for this pest.

Effect of a near-zero magnetic field on development and flight of oriental armyworm (Mythimna separata)

The geomagnetic field affects all living organisms on the Earth. In this study we investigated the developmental and behavioral effects of rearing Mythimna separata in a near-zero magnetic field (<500 nT) compared to the local geomagnetic field (approximately 50 µT). The near-zero magnetic field produced by a Helmholtz coil system significantly lengthened larval and pupal development durations, increased male longevity, and reduced pupal weight, female reproduction, and the relative expression level of the vitellogenin (Vg) gene in newly emerged females. Moreover, the near-zero magnetic field had a considerable negative effect on the mating ratio of M. separata adults. In addition, the moths in the near-zero magnetic field displayed less flight activity late in the night than those in the Earth's normal geomagnetic field, indicating that the flight rhythm of M. separata may be affected by the near-zero magnetic field. Reduction in magnetic field intensity may have negative effects on the development and flight of oriental armyworm, with consequent additional effects on its migration.

Sugar-Acetic Acid-Ethanol-Water Mixture as a Potent Attractant for Trapping the Oriental Fruit Moth (Lepidoptera: Tortricidae) in Peach-Apple Mixed-Planting Orchards.

Sugar–acetic acid–ethanol–water mixture (SAEWM) trapping has initially shown the potential efficacy for monitoring or trapping insects. It is unknown how SAEWM-baited traps affect field number of oriental fruit moth (OFM), Grapholita molesta (Busck) (Lepidoptera: Tortricidae), the female/male ratio trapped, and the type of natural-enemy insects captured. This study investigated changes in seasonal population dynamics and diurnal flight rhythm of OFM, the number and female/male ratio of OFM and the numbers of Coccinellidae and Chrysopidae trapped by SAEWM in peach–apple mixed-planting orchards. The SAEWM performed well in trapping OFM, most of which were adult females, with the maximum trapping at 2.5 m above ground. The daily trapping peak occurred between 18:00 and 20:00, during each continuous monitoring period, with another peak occurring at 4:00–8:00, after the second monitoring period (2–5 July). However, the use of SAEWM also resulted in the trapping of Coccinellidae and Chrysopidae, of which peak trapping time partially overlapped with the second and third peak trapping times of OFM. We suggest the cessation of SAEWM trapping during the peak activity time of Coccinellidae and Chrysopidae, or application of alternative attractive mixture that do not trap the natural enemy insects, in order to protect the ecological balance in the field.

Non linear dynamics of mechanosensory flight control in flies

In most animals, rhythmic motion is governed by central pattern generators (CPGs) - neural circuits that generate periodic patterned output. Sensory input to the CPG is not necessary to maintain the periodic neural activity, but is known to strongly influence it. For example, proprioceptive afferent input may entrain the neural CPG rhythm to the mechanical resonance frequency of a limb [1]. CPGs have been shown to govern the locomotor rhythms in vertebrates as well as in insects. A CPG governing the flight rhythm, however, has not been identified in flies, which are known for their remarkable flight maneuverability. In flies, the wingbeat rhythm is generated myogenically by stretch-activated power muscles and hence is not directly controlled by neural input. It is therefore unclear if the insights gained for proprioceptive feedback in CPG-based motor systems [1] likewise apply to flight control in flies. In our study, we investigated if and how proprioceptive feedback influences the rhythm of the myogenic wing beat oscillator. We concentrated on mechanosensory input from the halteres - specialized „gyroscopic sensory organs of flies. The halteres are known to activate the motor neurons of miniscule steering muscles, which in turn modulate the motion of the wings. In our experiments [2], tethered flying fruit flies (Drosophila melanogaster) were vibrated by a piezoelectric actuator to stimulate the haltere mechanosensory pathways. We used a laser Doppler interferometer to measure the vibrations of the tether resulting from the superposition of the piezo-delivered stimulus and the fly's wing beat. We determined the phase relationship between the wing motion and the mechanical stimulus in each wing stroke and applied an automated synchrogram analysis [3] to detect entrainment and higher-order synchronization. The flies synchronized with the stimulus for specific ranges of stimulus amplitude and frequency, revealing the characteristic Arnol'd tongues of a forced limit cycle oscillator. Our analysis shows that the steering muscles (activated by proprioceptive input) act as a mechanical forcing of the central power muscle oscillator. We propose that the mechanical forcing of a myogenic limit cycle oscillator permits flies to avoid the comparatively slow control based on a neural central pattern generator. In the entrainment study described above, flies were attached to tethers with high resonance frequency and damping coefficient. While experimenting with tethers of varying mechanical properties, however, we observed that the fly's behavior was significantly influenced by the properties of the tether. To systematically explore this influence for a given fly, we altered the tether's resonance frequency by clamping the tether at a different point in each distinct flight test. In these experiments, no piezo stimulus was applied. Yet, when the tether resonance frequency was comparable to the wing beat frequency, the forces from the fly lead to large cumulative motion of the tether and activation of the haltere mechanosensors. The fly therefore received delayed feedback dependent on its previous activity. This lead to a variety of observed dynamical regimes, including the locking of the wing beat frequency to the tether resonance frequency when their initial difference was sufficiently small (similar to limb entrainment in [1]). We were able to reproduce most of the observed dynamical features in a simplified mathematical model of two mutually coupled oscillators: a phase-reduced nonlinear oscillator representing the wing beat and a linear oscillator representing the tether dynamics.

Flight and Walking in Locusts–Cholinergic Co-Activation, Temporal Coupling and Its Modulation by Biogenic Amines

Walking and flying in locusts are exemplary rhythmical behaviors generated by central pattern generators (CPG) that are tuned in intact animals by phasic sensory inputs. Although these two behaviors are mutually exclusive and controlled by independent CPGs, leg movements during flight can be coupled to the flight rhythm. To investigate potential central coupling between the underlying CPGs, we used the muscarinic agonist pilocarpine and the amines octopamine and tyramine to initiate fictive flight and walking in deafferented locust preparations. Our data illustrate that fictive walking is readily evoked by comparatively lower concentrations of pilocarpine, whereas higher concentrations are required to elicit fictive flight. Interestingly, fictive flight did not suppress fictive walking so that the two patterns were produced simultaneously. Frequently, leg motor units were temporally coupled to the flight rhythm, so that each spike in a step cycle volley occurred synchronously with wing motor units firing at flight rhythm frequency. Similarly, tyramine also induced fictive walking and flight, but mostly without any coupling between the two rhythms. Octopamine in contrast readily evoked fictive flight but generally failed to elicit fictive walking. Despite this, numerous leg motor units were recruited, whereby each was temporarily coupled to the flight rhythm. Our results support the notion that the CPGs for walking and flight are largely independent, but that coupling can be entrained by aminergic modulation. We speculate that octopamine biases the whole motor machinery of a locust to flight whereas tyramine primarily promotes walking.

Effect of Trap Size, Trap Height and Age of Lure on SamplingXyleborus glabratus(Coleoptera: Curculionidae: Scolytinae), and its Flight Periodicity and Seasonality

Xyleborus glabratus (Coleoptera: Curculionidae: Scolytinae) is a non-native pest that transmits the causal pathogen of laurel wilt disease to plants belonging to the Lauraceae. To improve the current monitoring and survey techniques of X. glabratus, various trapping and flight behavior studies were conducted in natural areas with host species in Alachua County, Florida. Daylight flight rhythm studied at Austin Cary Memorial Forest twice in Sep 2010 using sticky traps baited with manuka lures showed that X. glabratus flies mostly between 1600 and 1800 h daylight saving time. Flight height of the beetle was determined in a trapping study using ladder-like traps. The largest number of beetles was trapped at heights of 35–100 cm above the ground. Seasonality of X. glabratus was studied in Florida from Mar 2010–Dec 2011. Three peaks of trap catches occurred during Apr 2010, Oct 2010 and Mar 2011. To find the optimal Lindgren funnel trap design for X. glabratus, a study was conducted using 4, 8, 12 and 16 funnels per trap. Funnel traps with 8, 12, 16 funnels per trap captured similar numbers of X. glabratus, but significantly more than with 4 funnels per trap. The effect of aging of manuka lures was studied at 2 different sites in Alachua County, Florida. New manuka lures trapped significantly more X. glabratus than lures aged 2, 4 and 6 wk. Trap color, whether black, white, blue, yellow, red or transparent, had no significant influence on the number of X. glabratus trapped.

Frequency Control of Motor Patterning by Negative Sensory Feedback

The sensory system plays a key role in the generation of behavior by providing the nervous system with information about the environment and feedback about body movements such that motor output can continuously be adapted to changing circumstances. Although the effects of sensory organs on nervous system function have been demonstrated in many systems, the impact of sensory activity has rarely been studied in conditions in which motor output and sensory activity can interact as they do in behaving animals. In such situations, emergent properties may surface and govern the characteristics of the motor system. We studied the dynamics of sensorimotor interaction with a combination of electrophysiological experiments and computational modeling in the locust flight pattern generator, including its sensory components. The locust flight motor output is produced by a central pattern generator that interacts with phasic sensory feedback from the tegula, a proprioceptor that signals downstroke movement of the wing. We modeled the flight control system, and we tested the model predictions by replacing tegula feedback in the animal with artificial feedback through computer-controlled electric stimulation of the appropriate sensory nerves. With reference to the cycle frequency in the locust flight rhythm, our results show that motor patterns can be regulated via the variation of sensory feedback loops. In closed-loop conditions, tegula feedback strength determines cycle frequency in the model and the biological preparation such that stronger feedback results in lower frequencies. This regulatory mechanism appears to be a general emergent property of negative feedback systems.

Reconfiguration of the respiratory network at the onset of locust flight.

Reconfiguration of the respiratory network at the onset of locust flight. J. Neurophysiol. 80: 3137-3147, 1998. The respiratory interneurons 377, 378, 379 and 576 were identified within the suboesophageal ganglion (SOG) of the locust. Intracellular stimulation of these neurons excited the auxillary muscle 59 (M59), a muscle that is involved in the control of thoracic pumping in the locust. Like M59, these interneurons did not discharge during each respiratory cycle. However, the SOG interneurons were part of the respiratory rhythm generator because brief intracellular stimulation of these interneurons reset the respiratory rhythm and tonic stimulation increased the frequency of respiratory activity. At the onset of flight, the respiratory input into M59 and the SOG interneurons was suppressed, and these neurons discharged in phase with wing depression while abdominal pumping movements remained rhythmically active in phase with the slower respiratory rhythm (Fig. ). The suppression of the respiratory input during flight seems to be mediated by the SOG interneuron 388. This interneuron was tonically activated during flight, and intracellular current injection suppressed the respiratory rhythmic input into M59. We conclude that the respiratory rhythm generator is reconfigured at flight onset. As part of the rhythm-generating network, the interneurons in the SOG are uncoupled from the rest of the respiratory network and discharge in phase with the flight rhythm. Because these SOG interneurons have a strong influence on thoracic pumping, we propose that this neural reconfiguration leads to a behavioral reconfiguration. In the quiescent state, thoracic pumping is coupled to the abdominal pumping movements and has auxillary functions. During flight, thoracic pumping is coupled to the flight rhythm and provides the major ventilatory movements during this energy-demanding locomotor behavior.

Neural parameters contributing to temperature compensation in the flight CPG of the locust,Locusta migratoria

Elevated thoracic temperature increases the wingbeat frequency of flying locusts. We investigated the extent to which temperature-induced changes in resting membrane potential and postsynaptic potential amplitude contribute to the effects of increased temperature on the frequency of the central flight rhythm. Flight neurons were hyperpolarized by changing the K+ concentration of the superfusing saline from 10 mM to 2 mM. 5 min of low-K+ superfusion hyperpolarized flight motoneurons from −42.8 mV to −50.1 mV with a concomitant decrease of the frequency of the central flight rhythm from 11.6 Hz to 10.5 Hz. The amplitude of postsynaptic potentials was halved after 10 min of zero Ca2+/high Mg2+ superfusion, but the frequency of the central rhythm did not change significantly. GABAergic inhibitory connections were reduced in amplitude using picrotoxin. This treatment increased the frequency of the central rhythm from 11.6 Hz to 12.9 Hz, and increased the thermosensitivity of the rhythm frequency. We conclude that the excitatory effect of increased temperature on rhythm frequency is not mediated by temperature effects on membrane potential and/or synaptic potential amplitude. We propose that the inhibitory effect of temperature-induced hyperpolarization of the membrane potential compensates for the excitatory effect of temperature on rhythm frequency (e.g. via increased conduction velocity). We further suggest that some measure of temperature compensation is afforded by equal effects on the amplitudes of excitatory and inhibitory postsynaptic potentials, such that the net effect on the level of excitation is zero.

Exposure to heat shock affects thermosensitivity of the locust flight system.

The natural habitat of the migratory locust, Locusta migratoria, is likely to result in locusts being heat stressed during their normal adult life. It is known that locusts exhibit a heat-shock response: exposure to 45 degrees C for 3 h induces thermotolerance and the expression of heat-shock proteins. We investigated the effects of exposure to heat-shock conditions on the thermosensitivity of flight rhythm generation in tethered, intact animals and in deafferented preparations. Heat shock had no effect on wingbeat frequency measured at the start of flight sequences, nor did it affect the postimaginal maturation of this parameter. During sustained flight, heat shock slowed the characteristic asymptotic reduction of wingbeat frequency. Wingbeat frequency of heat-shocked animals was less sensitive to temperature in the range 24 degrees to 47 degrees C than that of control animals, and the upper temperature limit, above which flight rhythms could not be produced, was 6 degrees to 7 degrees C higher in heat-shocked animals. These results were mirrored in the response of deafferented preparations, indicating that modifications in the properties of the flight neuromuscular system were involved in mediating the response of the intact animal. We propose that exposure to heat shock had the adaptive consequences of reducing thermosensitivity of the neural circuits in the flight system and allowing them to operate at higher temperatures.

Wing-beat coupling between flying locust pairs: preferred phase and lift enhancement

Pairs of locusts flying in tandem in a wind tunnel are known to couple their wing-beats intermittently. The rhythmically oscillating air flow from the front locust's wing-beat, detected by the rear individual, appears to convey the timing information for coupling. Three predictions of this arrangement were tested quantitatively in this study. (1) Given that the oscillating air flow has a wavelength of 7.5 cm, placing the rear locust 7.5 or 15 cm behind the front one should produce the same phase of coupling, whereas placing it at an intermediate distance of 11 cm should produce an opposite phase. (2) At any distance, the preferred phase at which wing-beat coupling occurs should depend, in part, on the difference in the wing-beat frequencies of the two locusts just before the coupling began. (3) At the moment that the wing-beats of the two locusts become coupled, a change should be observed consistently in the wing-beat frequency of the rear individual only. Each of these three predictions was fulfilled. We also recorded the instantaneous lift of the rear locust by tethering it to a laser torque meter. Lift varied with the phase of the wing-beats between the two locusts. For a given distance between the two locusts, lift was greater by a mean of 16 % of the locust's body mass at those phases where coupling most commonly occurred than at opposite phases. This lift effect was seen even if the wing-beats of the two locusts drifted through these preferred phases without actually coupling. These results are discussed in terms of a possible energetic advantage conferred to the rear locust by flying in tandem and by coupling its flight rhythm to the leader's wing-beat.

Effects of maturation on synaptic potentials in the locust flight system

We have measured parameters of identified excitatory postsynaptic potentials from flight interneurons in immature and mature adult locusts (Locusta migratoria) to determine whether parameters change during imaginal maturation. The presynaptic cell was the forewing stretch receptor. The postsynaptic cells were flight interneurons that were filled with Lucifer Yellow and identified by their morphology. Excitatory postsynaptic potentials from different postsynaptic cells had characteristic amplitudes. The amplitude, time to peak, duration at half amplitude and the area above the baseline of excitatory postsynaptic potentials did not change with maturation. The latency from action potentials in the forewing stretch receptor to onset of excitatory postsynaptic potentials decreased significantly with maturation. We suggest this was due to an increase in conduction velocity of the forewing stretch receptor. We also measured morphological parameters of the postsynaptic cells and found that they increased in size with maturation. Growth of the postsynaptic cell should cause excitatory postsynaptic potential amplitude to decrease as a result of a decrease in input resistance, however, this was not the case. Excitatory postsynaptic potentials in immature locusts depress more than in mature locusts at high frequencies of presynaptic action potentials. This difference in frequency sensitivity of the immature excitatory postsynaptic potentials may account in part for maturation of the locust flight rhythm generator.

Activity of the forewing stretch receptor in immature and mature adult locusts

Maturation of the flight system of Locusta migratoria occurs during the first two weeks following imaginal ecdysis. One aspect of maturation is an increase in the wingbeat frequency from about 13 Hz to about 23 Hz. We investigated physiological and anatomical mechanisms that may contribute to this process. The difference between the frequencies of the central flight rhythms of immature and mature deafferented preparations was not as great as that between the wingbeat frequencies of immature and mature intact animals. Results from static and dynamic wing elevation showed that the intensity of the forewing stretch receptor response to a given stimulus increased during maturation. The diameter of the main stretch receptor axon was larger and the conduction velocity of signals conveyed along the forewing stretch receptor and the dorsal longitudinal motoneuron was faster in mature than in immature animals. We conclude that during maturation of the flight system the forewing stretch receptor responds to wing elevation with a higher frequency signal that reaches the central circuitry faster. These findings are discussed in the context of a model that describes the influence of stretch receptor input on wingbeat frequency along with other potential mechanisms involved in flight maturation.

The locust tegula: significance for flight rhythm generation, wing movement control and aerodynamic force production

The tegula, a complex sense organ associated with the wing base of the locust, plays an important role in the generation of the flight motor pattern. Here its function in the control of wing movement and aerodynamic force production is described. The vertical component of forewing movement was monitored while recording intracellularly from flight motoneurones during stationary flight. First, in accordance with previous electrophysiological results, stimulation of hindwing tegula afferents was found to reset the wingstroke to the elevation phase in a well-coordinated manner. Second, recordings made before and after removal of fore- and hindwing tegulae were compared. This comparison demonstrated that the delayed onset of elevator motoneurone activity caused by tegula removal is accompanied by a corresponding delay in the upstroke movement of the wings. The consequences of this delayed upstroke for aerodynamic force production were investigated by monitoring wing movements and lift generation simultaneously. A marked decrease in net lift generation was observed following tegula removal. Recordings of wing pronation indicate that this decrease in lift is primarily due to the delayed upstroke movement - that is, to a delay of the wings near the aerodynamically unfavourable downstroke position. It is concluded that the tegula of the locust hindwing signals to the nervous system the impending completion of the wing downstroke and allows initiation of the upstroke movement immediately after the wings have reached the lower reversal point of the wingstroke. The functional significance of tegula feedback and central rhythm generation for locust flight control are discussed.

The Locust Tegula: Significance for Flight Rhythm Generation, Wing Movement Control and Aerodynamic Force Production

ABSTRACT The tegula, a complex sense organ associated with the wing base of the locust, plays an important role in the generation of the flight motor pattern. Here its function in the control of wing movement and aerodynamic force production is described. The vertical component of forewing movement was monitored while recording intracellularly from flight motoneurones during stationary flight. First, in accordance with previous electrophysiological results, stimulation of hindwing tegula afferents was found to reset the wingstroke to the elevation phase in a well-coordinated manner. Second, recordings made before and after removal of fore-and hindwing tegulae were compared. This comparison demonstrated that the delayed onset of elevator motoneurone activity caused by tegula removal is accompanied by a corresponding delay in the upstroke movement of the wings. The consequences of this delayed upstroke for aerodynamic force production were investigated by monitoring wing movements and lift generation simultaneously. A marked decrease in net lift generation was observed following tegula removal. Recordings of wing pronation indicate that this decrease in lift is primarily due to the delayed upstroke movement – that is, to a delay of the wings near the aerodynamically unfavourable downstroke position. It is concluded that the tegula of the locust hindwing signals to the nervous system the impending completion of the wing downstroke and allows initiation of the upstroke movement immediately after the wings have reached the lower reversal point of the wingstroke. The functional significance of tegula feedback and central rhythm generation for locust flight control are discussed.

The activity of pleurodorsal muscles during flight and at rest in the moth Manduca sexta (L.)

In the moth Manduca sexta, the paired mesothoracic flight steering muscle II PD2m takes part in the generation of the flight rhythm and is spontaneously active in the non-flying animal. This spontaneous activity is modulated by optomotor stimuli and directionally selective. The directional response characteristics are analyzed. Another spontaneously active steering muscle pair, the III PD2c, is situated in the metathorax. The activities of this pair and of a third muscle pair, the III PD3 are also influenced by visual stimulation. The responses of all 6 muscles to optomotor stimuli which simulate the flight situations yaw, roll, thrust and lift are analyzed. Each situation elicits a unique pattern of activation/deactivation within this set of muscles. The activity pattern in non-flying animals allows the prediction of flight steering mechanisms such as changes of wing area in flight turns and provides a useful basis for the analysis of visuo-motor pathways.

Delayed excitatory connections in the flight system of the locust

1. Synaptic interactions between identified neurons in the flight system of the locust were investigated by the use of standard intracellular recording and staining techniques. The intent was to determine the distribution and functional significance of delayed excitatory connections, which have been previously described. 2. For one inhibitory connection it was demonstrated that subthreshold depolarization of the presynaptic neuron was sufficient to cause release of transmitter at the synapse. This established the existence of graded interactions between spiking flight neurons. 3. Three inhibitory interneurons were found to cause delayed excitatory responses in several other neurons. Often these were coupled with direct inhibitory connections between the same pre- and postsynaptic neurons, resulting in an inhibitory/excitatory (I/E) postsynaptic potential (PSP). The two phases of this PSP were variable. 4. Delayed excitatory connections appeared powerful while the flight system was inactive. However, these connections were disabled during flight rhythms at the phase when the presynaptic neuron was depolarized and firing action potentials. This was likely to be due to the nature of the disynaptic disinhibitory interaction being via (an) intervening neuron(s) with oscillating membrane potentials and thresholds for release of transmitter. 5. Thus connections demonstrated when flight rhythms were not expressed changed their character during flight rhythms. The delayed excitatory connections in this system probably reflect complex circuits of inhibition mediated by graded interactions and have little functional significance as phenomena in their own right.

Digging activity by the oriental hornet (Vespa orientalis; Hymenoptera, Vespinae) is correlated with solar radiation

Observations were made on the activities of workers of the Oriental hornetVespa orientalis, during flight to and from the nest, on fully active days in months of maximal colony activities. Two types of flight out of the nest were recorded: flight for removal of dug-up soil and flight for foraging of buiding materials and food from the field. The flights of digger workers occur and peak around 1200, (with even slopes down to zero on both sides of the peak). The flight activity curve is gaussian and in accordance with the intensity of solar irradiation. Flight activities of foraging workers are limited in the morning hours but subsequently increase, the curve resembling that of the air temperature at 2m above the soil surface. The flight rhythm of digger hornets in the presence of 2 adjacent outles and the rhythm of activity of digger hornets of 2 abutting nests were also investigated. The results indicate a strong competition among the diggers for flight opportunity during periods of highest insolation intensity. Due to the correlation between the flight of digger hornets and the intensity of sun radiation, it is assumed that hornets do make use of solar energy for flight purposes.

Neural Mechanisms Underlying Axial/Appendicular Steering Reactions in Locust Flight

SYNOPSIS. Steering during flight in the locust involves complex changes in wingbeat, bending of thorax and head, and ruddering movements of abdomen and hindlegs. Most of these behavioral subcomponents involve coordinated modification of axial and appendicular musculature control. Some of the mechanisms underlying this neural modification have been analysed at the cellular level. During steering via wingbeat, sensory information about course deviations leads to highly coordinated and asymmetric changes in the flight motor's output through the following mechanisms. Identified feature detector neurons in the locust brain integrate sensory information concerning specific types of course deviation. Each of these descending detector neurons makes connections with a population of thoracic interneurons. These thoracic interneurons have two important properties. First, they relay deviation information to flight motoneurons. Second, they are under the gating control of the flight central oscillator. Through this gating control the descending sensory signal is phase-coupled to the flight rhythm and delivered to appropriate flight motoneurons in one and the same step. Although most of the recent cellular studies have been aimed at unraveling the neural basis of wingbeat alterations, similar (but not identical) principles of neural organization seem to be involved in the steering reactions produced by axial motor systems.

Multiple feedback loops in the flying cockroach: excitation of the dorsal and inhibition of the ventral giant interneurons.

1. In a tethered cockroach (Periplaneta americana) whose wings have been cut back to stumps, it is possible to elicit brief sequences of flight-like activity by puffing wind on the animal's body. 2. During such brief sequences, rhythmic bursts of action potentials coming from the thorax at the wingbeat frequency, descend the abdominal nerve cord to the last abdominal ganglion (A6). This descending rhythm is often accompanied by an ascending rhythm (Fig. 2). 3. Intracellular recording during flight-like activity from identified ascending giant interneurons, and from some unidentified descending axons in the abdominal nerve cord, shows that: (a) ventral giant interneurons (vGIs) remain silent (Fig. 3); (b) dorsal giant interneurons (dGIs) are activated at the onset of the flight-like activity and remain active sporadically throughout the flight sequence (Fig.4); (c) some descending axons in the abdominal nerve cord show rhythmic activity phase-locked to the flight rhythm (Fig. 5). 4. Also during such brief sequences, the cercal nerves, running from the cerci (paired, posterior, wind sensitive appendages) to the last abdominal ganglion, show rhythmic activity at the wingbeat frequency (Fig. 6). This includes activity of some motor axons controlling vibratory cercal movements and of some sensory axons. 5. More prolonged flight sequences were elicited in cockroaches whose wings were not cut and which flew in front of a wind tunnel (Fig. 1B). 6. In these more prolonged flight sequences, the number of ascending spikes per burst was greater than that seen in the wingless preparation (Fig. 8; compare to Fig. 2). Recordings from both ventral and dorsal GIs show that: in spite of the ongoing wind from both the tunnel and the beating wings, which is far above threshold for the vGIs in a resting cockroach, the vGIs are entirely silent during flight. Moreover, the vGIs response to strong wind puffs that normally evoke maximal GI responses is reduced by a mean of 86% during flight (Fig. 9). The dGIs are active in a strong rhythm (Figs. 11 and 12). 7. Three sources appear to contribute to the ascending dGI rhythm (1) the axons carrying the rhythmic descending bursts; (2) the rhythmic sensory activity resulting from the cercal vibration; and (3) the sensory activity resulting from rhythmic wind gusts produced by the wingbeat and detected by the cerci. The contribution of each source has been tested alone while removing the other two (Figs. 13 and 14). Such experiments suggest that all 3 feedback loops are involved in rhythmically exciting the dGIs (Fig. 15).