Wolfram Kutsch

A reconsideration of the central pattern generator concept for locust flight

SummaryAlthough it is generally agreed that locusts can generate flight similar rhythmic motor activity in the absence of sensory feedback from the wings, recent studies indicate that functional deafferentation produces significant changes in the flight motor pattern (Hedwig and Pearson 1984). These findings have raised doubts on the adequacy of the central pattern generator concept for the locust flight system (Pearson 1985). In this paper, we re-investigate the effects of deafferentation on the capacity of adult migratory locusts to generate the flight motor pattern. For this purpose, the experimental animals were dissected to various degrees, ranging from head-ventral nerve cord, to isolated pterothoracic nerve cord, and finally single isolated ganglion preparations. Flight motor activity was released by either wind stimulation, the more traditional method, or by applying octopamine (Sombati and Hoyle 1984; Stevenson and Kutsch 1986). In all cases the released motor activity was analysed, giving details of latency, and phase relationships between specific synergistic and antagonistic motor units, and then compared with the flight motor pattern generated by intact tethered locusts.This analysis shows that deafferentation, although reducing the frequency, does not necessarily disrupt the basic flight motor pattern. By using octopamine we could show that even isolated thoracic nerve cord preparations can generate activity, which in all major aspects corresponds to this motor program. This could also be shown for the fully isolated metathoracic ganglion and we provide some evidence that the mesothoracic ganglion may be capable of a similar performance. In addition to releasing flight activity, octopamine was also found to enhance the responsiveness of deafferentated locusts to wind stimulation. This resulted in a considerable elevation of the frequency and prolongation of the flight motor activity to values comparable to the performance of intact tethered locusts.

Homologous Structures in the Nervous Systems of Arthropoda

Publisher Summary This chapter deals with the homologous structures in the nervous systems of Arthropoda. The Arthropoda constitute the phylum with the highest diversity of species in the animal kingdom. Originated in the Precambrium, this monophylum basically consists of two groups, the Chelicerata and the Mandibulata. The common ancestor of the arthropods has to be regarded as an annelid-like species, with an exoskeleton, serial homologous segments bearing a series of repetitively structured appendages, and possessing fused “head”-segments in the anterior region. Recent fossil evidence has debilitated an alternative view, the uniramian concept which regards the Arthropoda as a polyphylum. According to the concept of an arthropod monophylum, compartments of the nervous system reveal some of the synapomorphies of this phylum. The Onychophora represent a taxon which is regarded to have evolved convergently to the arthropod phylum. This chapter explores new evidences that suggest they are a sister-group of the Chelicerata. Peripatus has a brain with several similarities to neuropile regions in the spider brain, for example the “mushroom bodies” and the “central body”.

Demonstration of functional connectivity of the flight motor system in all stages of the locust

SummaryThe development of the flight motor pattern was studied by recording from the thoracic muscles of locusts of various developmental stages. In response to a short wind stimulus, larval locusts generate unpatterned motor activity, whereas newly moulted adults generate the flight pattern (Fig. 1A). The latter is equivalent to the mature adult flight pattern, although more irregular and of lower frequency. Experiments with highly deafferentated locusts indicate that the switch from the larval tonic to adult phasic flight pattern and subsequent increase in frequency are not dependent on phasic peripheral feedback from moving body structures (Fig. 1B). By using octopamine, flight motor activity could be released without need of the wind stimulus (Fig. 2). This corresponded to the normal wind released flight pattern of intact locusts, although the frequency was lower (Fig. 8). Following octopamine treatment, the response to wind stimulation was enhanced. Wind then released in deafferentated adults long flight sequences of significantly elevated frequency (Fig. 3). Although flight is essentially an adult specific behaviour, octopamine was finally found to release flight motor activity in all larval stages (Fig. 7).We conclude that major steps in the development of the flight motor circuitry are completed by the end of embryogenesis. Thus, in contrast to previous assumptions (cf. Bentley and Hoy 1970; Kutsch 1974a; Altman 1975), postembryonic changes in neither the central, nor peripheral nervous system appear to be of major importance for the ontogeny of the locust flight motor program. Whether developmental changes in the wind sensory system of the head, or levels of neurohormones such as octopamine, are related to the newly acquired responsiveness of freshly moulted adult locusts to the normal flight releasing stimulus is discussed.

The influence of the wing sense organs on the flight motor pattern in maturing adult locusts

SummaryImmediately after destruction of the sense organs in the wings and wing-hinges, the wing-beat frequency of matureLocusta migratoria decreases to 50–60% of the initial value. During the following days the frequency increases again. Similar results were obtained with young adult locusts. The same operation immediately after the last ecdysis does not prevent the appearenee of the normal flight pattern. The increase of the frequency during the first weeks of adult life is about the same in operated and non-operated locusts. Muscle recordings of old and young adults show similar changes of the flight motor pattern after destruction of the wing receptors. The results indicate that the development of the flight motor program is not dependent on wing afferents. The commands of the wing sense organs raise the frequency of the central flight oscillator by the same amount in both young and old adult locusts.

The influence of age and culture-temperature on the wing-beat frequency of the migratory locust, Locusta migratoria

Abstract Starting on the day of adult ecdysis, the wing-beat frequency of Locusta migratoria rises exponentially. The initial frequency for both sexes is ca. 10 Hz, and the final frequency for males (24–25 Hz) is somewhat higher than for females (ca. 21 Hz). Initial and final frequencies appear to be genetically programmed, because they are independent of the culture cage temperature and amount of flight experience. The rate at which the final frequency is attained, however, is culture temperature dependent, being faster when the temperature is higher. After having reached the final frequency the wing-beat changes only a little up to the time of the animals death.

Time-correlated flights of juvenile and mature locusts: A comparison between free and tethered animals

Abstract The flights of free and tethered Locusta migratoria were followed from initiation with a high-speed film camera. A longer sequence of wing-beat cycles can thus be correlated unequivocally with the animalss movement in time and space. In both flight situations the locusts start with approximately the same instantaneous wing-beat frequency. During the early flight phase free-flying animals increase their wing-beat frequency, whereas for tethered locusts this parameter remains constant or even decreases. The general flight pattern is similar in juvenile and mature locusts; the juveniles however, fly with alower wing-beat frequency and flight speed. The differences in the wing-beat frequencies for both flight performances are discussed with respect to differences in the sensory inputs to the flight motor centre.

Development of flight behaviour in maturing adults of Locusta migratoria: II. Aerodynamic parameters

Abstract In Locusta migratoria suspended from a flight balance, flight speed relative to the air and the lift were recorded throughout adult life. During continuous flight at all ages flight speed and lift decrease, but during maturation both aerodynamic parameters increase. These parameters appear to be dominated by the wing-stroke frequency in a more or less constant relationship. Locusts only 2 days old can maintain altitude in free flight. It is concluded that the basic neuronal flight pattern is determined at the last moult and that only the motoroutput frequency increases to approximately match the body weight, which increases with age.

Pre-imaginal flight motor pattern in Locusta

Abstract In a wind stream, larval stages of Locusta usually show a tonic muscle activity but they can also exhibit a rhythmic motor output. With ageing such a pattern can be released sooner, the trains become longer. The basic rhythm of 10 Hz does not change. The initial co-contraction of specific muscles is substituted later in development by an antagonistic recruitment. This activity resembles the flight motor pattern of young locusts which lack phasic sensory feedback from the wing region. Azadirachtin, an insect growth regulator, has been used to produce a permanent 5th larval instar. However, the extension of the last larval stage does not lead to a further development of the motor pattern to a level comparable to mature animals.

Transmission of muscle potentials during free flight of locusts

Abstract This paper briefly outlines developments in light-weight telemetry devices, and describes in detail a miniature radio system that transmits muscle potentials from the desert locust, Schistocerca gregaria, in free flight. The device, which is mounted to the insects prothorax weighs only about 10% of its bodys mass, and does not restrict the locusts ability to fly and to manoeuvre normally. When combined with video-monitoring, both normal (=50 Hz) or high-speed frame frequency (up to 500 Hz), the system makes it possible to record the electrical activity of certain muscles (EMG) and to compare this activity with the insects behavioural performance. Results are presented that show that the electrical activity can be associated with several flight parameters, e.g. flight speed, wing-beat frequency, wing-stroke angles, and rotations about different body axes. The recent advent of even smaller electronic parts has made possible the realisation of multi-channel transmission, and a dual-channel device has been successfully used to simultaneously record two physiological parameters from a flying locust. This device demonstrated the recruitment of bilateral symmetric muscles during yawing or rolling, and allowed the timing of homonomous muscle action to be recorded. Some of the results are novel, and others generally corroborate earlier findings derived from tethered animals. It is expected that further advances in the miniaturisation of electronic components will make telemetry from smaller insects a possibility in the future.

Ontogenetic studies of flight initiation in Locusta: Wind response of an identified interneurone (TCG)

Abstract The tritocerebral commissure giant (TCG) wind-sensitive interneurone is involved in initiation and maintenance of flight in adult locusts. In this paper we study this interneurone in the imago and non-flying larval instars. Cobalt fills show that the TCG establishes its adult morphology by the first larval instar. An accompanying axon, apparently representing the peculiar tritocerebral commissure “dwarf” (TCD) is present, too, at least for the last preimaginal instars. Physiological tests show similar responses of the TCG to wind stimuli in the 4th, 5th instar and adult stages. Spike activity, however, is usually higher in adult compared to larval instars. It is possible that all interneurones, involved in adult-specific motor patterns (such as flight), are present in preimaginal stages and can be activated independently of the function of the final motor system.