Summary
The activity of flight interneurons was recorded intracellularly in intact, tethered flying locusts (Locusta migratoria) and after removal of sensory input from the wing receptors. Depolarization patterns and spike discharges were characterized and compared for the two situations.
In general, depressor interneurons (n=6) showed only minor changes in their activity as a result of deafferentation (Fig. 1). Exceptions were interneurons 308 and 506 (Fig. 2). By contrast, all but one of the elevator interneurons (n=9) produced distinctly different depolarization patterns in intact locusts and following deafferentation. Three different groups of elevator interneurons were found (excluding the one exceptional neuron, Fig. 6). (i) One group of interneurons (n=4) produced different, superthreshold depolarizations in intact and deafferented animals (Fig. 3). Characteristic, biphasic depolarizations were recorded from these fibres at lower wingbeat frequencies in the intact situation but only single, delayed potentials were recorded after deafferentation. (ii) The second group of interneurons (n=3) exhibited distinct rhythmic activity only in intact animals. After deafferentation their depolarizations were small and often below the threshold for spike initiation (Fig. 4). (iii) One interneuron produced rhythmic flight motor oscillations only after deafferentation. In intact locusts the membrane potential of this neuron showed very small oscillations and remained subthreshold (Fig. 5).
Four main conclusions emerge from these data. (i) The activity of elevator interneurons is under greater sensory control than that of the depressors. This confirms the results of our previous electromyographic and motoneuronal analyses, (ii) A considerable portion of elevator activity is generated as a result of phasic sensory feedback. An essential input is from the hindwing tegulae (Table 1; Pearson and Wolf 1988). (iii) The activity of depressor interneurons appears to be determined by central mechanisms to a major extent. (iv) Different sets of central neurons appear to be involved in flight pattern generation in intact and deafferented locusts —although the two sets share many common elements.
Similar content being viewed by others
Abbreviations
- EMG :
-
electromyogram
- PSP :
-
postsynaptic potential (EPSP excitatory andIPSP inhibitory)
References
Altman JS, Anselment E, Kutsch W (1978) Postembryonic development of an insect sensory system: ingrowth of axons from the hindwing sense organs inLocusta migratoria. Proc R Soc London 202:497–516
Andersson O, Forssberg H, Grillner S, Lindquist M (1978) Phasic gain control of the transmission in cutaneous reflex pathways to motoneurons during ‘fictive’ locomotion. Brain Res 149:503–507
Bässler U (1986a) Afferent control of walking movements in the stick insectCunicula impigra. II. Reflex reversal and the release of the swing phase in the restrained foreleg. J Comp Physiol A 158:351–362
Bässler U (1986b) On the definition of central pattern generator and its sensory control. Biol Cybern 54:65–69
Bässler U, Wegener U (1983) Motor output of the denervated thoracic ventral nerve cord in the stick insectCarausius morosus. J Exp Biol 105:127–145
Boyan GS (1985) Auditory input to the flight system of the locust. J Comp Physiol A 156:79–91
Burrows M (1975) Monosynaptic connexions between wing stretch receptors and flight motoneurones of the locust. J Exp Biol 62:189–219
Forssberg H, Grillner S, Rossignol S (1975) Phase dependent reflex reversal during walking in chronic spinal acts. Brain Res 80:103–107
Getting PA, Dekin MS (1985)Tritonia swimming. A model system for integration within rhythmic motor systems. In: Selverston AI (ed) Model neural networks and behavior. Plenum Press, New York, pp 3–20
Getting PA, Lennard PA, Hume RI (1980) Central pattern generator mediating swimming inTritonia. I. Identification and synaptic interactions. J Neurophysiol 44:151–164
Grillner S (1985) Neurobiological bases of rhythmic motor acts in vertebrates. Science 228:143–149
Hasan Z, Stuart DG (1988) Animal solutions to problems of movement control. The role of proprioceptors. Annu Rev Neurosci 11:199–224
Horsmann U (1985) Der Einflu\ propriozeptiver Windmessung auf den Flug der Wanderheuschrecke und die Bedeutung descendierender Neuronen der Tritocerebralcommissur. PhD thesis, University of Cologne
Möhl B (1985a) The role of proprioception in locust flight control. II. Information signalled by forewing stretch receptors during flight. J Comp Physiol A 156:103–116
Möhl B (1985b) The role of proprioception in locust flight control. III. The influence of afferent stimulation of the stretch receptor nerve. J Comp Physiol A 156:281–291
Neumann L (1985) Experiments on tegula function for flight coordination in the locust. In: Gewecke M, Wendler G (eds) Insect locomotion. Parey, Hamburg, pp 149–156
Pearson KG, Robertson RM (1987) Structure predicts synaptic function of two classes of interneurons in the thoracic ganglia ofLocusta migratoria. Cell Tissue Res 250:105–114
Pearson KG, Wolf H (1987) Comparison of motor patterns in the intact and deafferented flight system of the locust. I. Electromyographic analysis. J Comp Physiol A 160:258–268
Pearson KG, Wolf H (1988) Connections of hindwing tegulae with flight neurones in the locust,Locusta migratoria. J Exp Biol 135:381–409
Reichert H, Rowell CHF (1985) Integration of nonphaselocked exteroceptive information in the control of rhythmic flight in the locust. J Neurophysiol 53:1201–1218
Reye DN, Pearson KG (1987) Projections of wing stretch receptors to central flight neurons in the locust. J Neurosci 7:2476–2487
Robertson RM, Pearson KG (1982) A preparation for the intracellular analysis of neural activity during flight in the locust. J Comp Physiol 146:311–320
Robertson RM, Pearson KG (1983) Interneurons in the flight system of the locust: distribution, connections and resetting properties. J Comp Neurol 215:33–50
Robertson RM, Pearson KG (1984) Interneuronal organization in the flight system of the locust. J Insect Physiol 30:95–101
Robertson RM, Pearson KG (1985a) Neural circuits in the flight system of the locust. J Neurophysiol 35:110–128
Robertson RM, Pearson KG (1985b) Neural networks controlling locomotion in locusts. In: Selverston AI (ed) Model neural networks and behavior. Plenum, New York, pp 21–35
Rossignol S, Lund JP, Drew T (1988) The role of sensory inputs in regulating patterns of rhythmical movements in higher vertebrates. In: Cohen A, Rossignol S, Grillner S (eds) Neural control of rhythmic movements in vertebrates. Wiley, New York, pp 201–283
Snodgrass RC (1929) The thoracic mechanism of a grasshopper and its antecedents. Smithson Misc Colins 82:1–111
Wendler G (1983) The locust flight system: functional aspects of sensory input and methods of investigation. In: Nachtigall W (ed) Biona report II. G Fischer, Stuttgart, pp 113–125
Wilson DM (1961) The central nervous control of flight in a locust. J Exp Biol 38:471–490
Wolf H, Pearson KG (1987a) Comparison of motor patterns in the intact and deafferented flight system of the locust. II. Intracellular recordings from flight motoneurons. J Comp Physiol A 160:269–279
Wolf H, Pearson KG (1987b) Intracellular recordings from interneurons and motoneurons in intact flying locusts. J Neurosci Methods 21:345–354
Wolf H, Pearson KG (1988) Proprioceptive input patterns elevator activity in the locust flight system. J Neurophysiol 59:1831–1853
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Wolf, H., Pearson, K.G. Comparison of motor patterns in the intact and deafferented flight system of the locust. J. Comp. Physiol. 165, 61–74 (1989). https://doi.org/10.1007/BF00613800
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00613800