Journal of comparative physiology

, Volume 150, Issue 4, pp 439–452 | Cite as

The tritocerebral commissure giant (TCG) wind-sensitive interneurone in the locust

I. Its activity in straight flight
  • Jonathan Bacon
  • Bernhard Möhl


  1. 1.

    The TCG interneurone of the locust (Schistocerca gregaria, Locusta migratoria) integrates information from the aerodynamic sense organs on the head, the wind hairs and the antennae. Its physiological characteristics and activity in the flying animal are analyzed using intracellular and extracellular methods.

  2. 2.

    Intracellular recording shows that TCG receives excitatory inputs from ipsilateral wind hairs in fields 2, 4 and 5 and from those in the posterior portion of field 1. Inhibitory inputs to the TCG originate from hairs in the anterior portion of field 1 and from all hairs of field 3. There are no contralateral inputs to the TCG (Figs. 3, 4). In addition, the ipsilateral antenna provides a weak, directionally selective input (Fig. 5).

  3. 3.

    The cell is rhythmically active in flight, firing in bursts in approximate synchrony with depressor muscle activity (Fig. 7). The bursting activity originates from rhythmic wind turbulences in front of the head, caused by the beating of the wings and by the rhythmic head movements during flight. Excitatory and inhibitory inputs from the wind hairs and the antennae act in concert to produce the TCG's rhythm with its particular relationship to the flight-muscle activity (Fig. 10).

  4. 4.

    The wind hairs and the antenna — as measured by TCG activity — are maximally sensitive to turbulences at frequencies between 20 and 25 Hz. This corresponds to the natural flight frequency (Fig. 11).

  5. 5.

    Waxing over all the wind hairs and the antennae causes a reduction of the flight frequency. This is achieved largely by an increase of the depressor to elevator latency, whereas the elevator to depressor latency remains relatively unchanged (Fig. 12).

  6. 6.

    Electrical stimulation of the wind-hair sensory cells during flight, so as to mimic their natural stimulation, demonstrates the fast phasic influence of these sense organs on the flight motor. A single electrical stimulus to the wind hairs generally excites elevator motor neurones, causing their activity to be slightly advanced in time (compared to an unstimulated wing-beat interval). This effect varies quantitatively as a function of the stimulus timing within the wing-beat cycle. In contrast, depressor motor neurone activity is advanced when wind-hair stimulation occurs 6–15 ms before their normal activity and is retarded when stimuli are presented at 15–40 ms latency (Fig. 13). Single stimulus pulses are sufficient to reset the original wing beat rhythm by approximately 0.6 ms. This suggests that the wind-sensory system is a component of the flight-rhythm generator (Fig. 14).



Inhibitory Input Motor Neurone Wing Beat Schistocerca Gregaria Flight Motor 
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  1. Bacon J, Altman JS (1977) A silver intensification method for cobalt filled neurons in wholemount preparations. Brain Res 138:359–363Google Scholar
  2. Bacon J, Möhl B (1979) Activity of an identified wind interneurone in a flying locust. Nature 278:638–640Google Scholar
  3. Bacon J, Tyrer NM (1978) The tritocerebral commissure giant (TCG): A bimodal interneurone in the locust,Schistocerca gregaria. J Comp Physiol 126:317–325Google Scholar
  4. Bacon J, Tyrer NM (1979) Wind interneurone input to flight motor neurones in the locust,Schistocerca gregaria. Naturwissenschaften 66:116Google Scholar
  5. Burrows M (1975) Monosynaptic connexions between wing stretch receptors and flight motorneurons of the locust. J Exp Biol 62:189–219Google Scholar
  6. Camhi JM (1969) Locust wind receptors: I. Transducer mechanics and sensory response. J Exp Biol 50:335–348Google Scholar
  7. Fielden HH (1960) Transmission through the last abdominal ganglion of the dragonfly nymph,Anax imperator. J Exp Biol 37:832–844Google Scholar
  8. Gewecke M (1972) Atennen- und Stirn-Scheitelhaare vonLocusta migratoria L. als Luftströmungs-Sinnesorgane bei der Flugsteuerung. J Comp Physiol 80:57–94Google Scholar
  9. Gewecke M (1979) Central projections of antennal afferents for the flight motor inLocusta migratoria (Orthoptera: Acrididae). Entomol Gen 5:317–320Google Scholar
  10. Heinzel HG, Gewecke M (1979) Directional sensitivity of the antennal campaniform sensilla in locusts. Naturwissenschaften 66:212–213Google Scholar
  11. Horsmann U, Heinzel H-G, Wendler G (1983) The phasic influence of self-generated air current modulations on the locust flight motor. J Comp Physiol 150:427–438Google Scholar
  12. Kondo H (1978) Efferent system of the lateral ocellus of the dragonfly: Its relationship with ocellar afferent units, the compound eyes, and the wing sensory system. J Comp Physiol 125:341–349Google Scholar
  13. Möhl B, Bacon J (1983) The tritocerebral commissure giant (TCG) wind-sensitive interneurone in the locust. II. Directional sensitivity and role in flight stabilisation. J Comp Physiol 150:453–465Google Scholar
  14. Möhl B, Nachtigall W (1978) Proprioceptive input in the locust flight motor revealed by muscle stimulation. J Comp Physiol 128:57–65Google Scholar
  15. Murphey RK, Palka J (1974) Efferent control of cricket giant fibres. Nature 248:249–251Google Scholar
  16. Murphey RK, Palka J, Hustert R (1977) The cercus-to-giant interneuron system of crickets. II. Response characteristics of two giant interneurons. J Comp Physiol 119:285–300Google Scholar
  17. Neumann L, Möhl B, Nachtigall W (1982) Quick phase-specific influence of the tegula on the flight motor. Naturwissenschaften 69:393–394Google Scholar
  18. O'Shea M, Adams M (1981) Pentapeptide (Proctolin: Arg-Tyr-Leu-Pro-Thr) associated with an identified neuron. Science 213:567–569Google Scholar
  19. O'Shea M, Rowell CHF, Williams JLD (1974) The anatomy of the locust visual interneurone; the descending contralateral movement detector. J Exp Biol 60:1–12Google Scholar
  20. Pearson KG, Wong RKS, Fourtner CR (1976) Connexions between hair-plate afferents and motoneurones in the cockroach leg. J Exp Biol 64:251–266Google Scholar
  21. Pearson KG, Heitler WJ, Steeves JD (1980) Triggering of locust jump by multimodal inhibitory interneurons. J Neurophysiol 43:257–278Google Scholar
  22. Pflüger HJ, Tautz J (1982) Air movement sensitive hairs and interneurons inLocusta migratoria. J Comp Physiol 145:369–380Google Scholar
  23. Reichert H, Plummer MR, Hagiwara G, Roth R, Wine JJ (1981) Sensory characteristics of local neurons in the last abdominal ganglion of the crayfish. Soc Neurosci Abstr 7:252Google Scholar
  24. Robertson RM, Pearson K (1982) A preparation for the intracellular analysis of neuronal activity during flight in the locust. J Comp Physiol 146:311–320Google Scholar
  25. Rowell CHF (1971a) The orthopteran descending movement detector (DMD) neurones: A characterisation and review. Z Vergl Physiol 73:167–194Google Scholar
  26. Rowell CHF (1971b) Variable responsiveness of a visual interneurone in the free-moving locust, and its relation to behaviour and arousal. J Exp Biol 55:727–747Google Scholar
  27. Rowell CHF, Pearson KG (1982) Ocellar input to the flight motor system of the locust: Structure and function. J Exp BiolGoogle Scholar
  28. Sachs L (1969) Statistische Auswertungsmethoden. Springer, Berlin Heidelberg New YorkGoogle Scholar
  29. Simmons P (1980) A locust wind and ocellar brain neurone. J Exp Biol 85:281–294Google Scholar
  30. Smola U (1970a) Untersuchung zur Topographie, Mechanik und Strömungsmechanik der Sinneshaare auf dem Kopf der WanderheuschreckeLocusta migratoria. Z Vergl Physiol 67:382–402Google Scholar
  31. Smola U (1970b) Rezeptor- und Aktionspotentiale der Sinneshaare auf dem Kopf der WanderheuschreckeLocusta migratoria. Z Vergl Physiol 70:335–348Google Scholar
  32. Tyrer NM (1980) Transmission of wind information on the head of the locust to flight motor neurons. Adv Physiol Sci 23:557–571Google Scholar
  33. Tyrer NM, Bacon J, Davies CA (1979) Sensory projections from the wind-sensitive head hairs of the locustSchistocerca gregaria. Cell Tissue Res 203:79–92Google Scholar
  34. Waldron I (1968) The mechanism of coupling of the locust flight oscillator to oscillatory inputs. Z Vergl Physiol 57:331–347Google Scholar
  35. Weis-Fogh T (1949) An aerodynamic sense organ stimulating and regulating flight in locusts. Nature 164:873–874Google Scholar
  36. Weis-Fogh T (1956) Biology and physics of locust flight IV. Notes on sensory mechanisms in locust flight. Philos Trans R Soc Lond [Biol] 239:553–584Google Scholar
  37. Wendler G (1974) The influence of proprioceptive feedback on locust flight co-ordination. J Comp Physiol 88:173–200Google Scholar
  38. Wendler G (1978) The possible role of fast wing reflexes in locust flight. Naturwissenschaften 65:65Google Scholar
  39. Williams JLD (1975) Anatomical studies on the insect central nervous system: a ground plan of the mid-brain and an introduction to the central complex in the locust,Schistocerca gregaria (Orthoptera). J Zool 176:67–86Google Scholar
  40. Wilson DM (1961) The central nervous control of flight in a locust. J Exp Biol 38:471–490Google Scholar
  41. Wilson DM (1968) The nervous control of insect flight and related behaviour. Adv Insect Physiol 3:289–338Google Scholar
  42. Wilson DM, Wyman RJ (1965) Motor output patterns during random and rhythmic stimulation of locust thoracic ganglia. Biophys J 5:121–143Google Scholar
  43. Wohlers D, Huber F (1978) Intracellular recording and staining of cricket auditory interneurons inGryllus campestris (L.) andGryllus bimaculatus (de Geer.) J Comp Physiol 127:11–28Google Scholar
  44. Zarnack W, Möhl B (1977) Activity of the direct downstroke muscles ofLocusta migratoria (L.) during steering behaviour in flight. J Comp Physiol 118:215–233Google Scholar

Copyright information

© Springer-Verlag 1983

Authors and Affiliations

  • Jonathan Bacon
    • 1
  • Bernhard Möhl
    • 2
  1. 1.Abteilung HuberMax-Planck-Institut für VerhaltensphysiologieSeewiesenFederal Republic of Germany
  2. 2.Arbeitsgruppe Nachtigall im Fachbereich Biologie der Universität des SaarlandesSaarbrückenFederal Republic of Germany

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