Journal of Comparative Physiology A

, Volume 196, Issue 3, pp 199–211 | Cite as

Synchronization of wing beat cycle of the desert locust, Schistocerca gregaria, by periodic light flashes

  • Fabian Schmeling
  • Gert Stange
  • Uwe Homberg
Original Paper


Studies on the generation of rhythmic motor patterns have shown that peripheral sensory input may contribute substantially to the rhythm generating network. A prominent example is the wing beat frequency of desert locusts, which can be entrained to rhythmic mechanosensory input, but also to the frequency of periodic light flashes. To further analyze the entrainment by light, tethered flying locusts were presented with periodic light flashes, while the position of the forewing was filmed. We show that entrainment of wing beat occurs both in the UV and green range of light. Animals maintained a characteristic phase relationship to the light stimulus with the most elevated wing position occurring at the end of the dark phase. Speed and time course of entrainment varied greatly and ranged from the duration of a single wing beat cycle to several seconds. To identify the visual system mediating entrainment, synchronization to UV light was tested after cutting the optic stalks to the optic lobes/compound eyes or the ocellar nerves. The results show that light entrainment of the locust flight pattern is largely and perhaps exclusively mediated via the fast ocellar pathway and may have a role to stabilize flight with respect to the horizon.


Insect flight Flight stabilization Central pattern generator Visual system Ocelli 



We thank Nicole Carey for assistance with MatLab and Richard Berry, Stanley Heinze, and Bianca Backasch for helpful discussions. This research was supported by Grants from the Air Force Office of Scientific Research, No. FA8655-08-C-3021 to U.H. and No. FA4869-06-1-0059 to G.S.


  1. Aschoff J, Wever R (1962) Über Phasenbeziehungen zwischen biologischer Tagesperiodik und Zeitgeberperiodik. Z Vgl Physiol 46:115–128CrossRefGoogle Scholar
  2. Ausborn J, Stein W, Wolf H (2007) Frequency control of motor patterning by negative sensory feedback. J Neurosci 27:9319–9328CrossRefPubMedGoogle Scholar
  3. Berger S, Kutsch W (2003) Turning manoevres in free-flying locusts: high-speed video-monitoring. J Exp Zool A299:127–138CrossRefGoogle Scholar
  4. Bergou AJ, Xu S, Wang ZJ (2007) Passive wing pitch reversal in insect flight. J Fluid Mech 591:321–337CrossRefGoogle Scholar
  5. Berry RP, Warrant EJ, Stange G (2007) Form vision in the insect dorsal ocelli: an anatomical and optical analysis of the locust ocelli. Vis Res 47:1382–1393CrossRefPubMedGoogle Scholar
  6. Briscoe AD, Chittka L (2001) The evolution of color vision in insects. Annu Rev Entomol 46:471–510CrossRefPubMedGoogle Scholar
  7. Buck J (1988) Synchronous rhythmic flashing of fireflies. II. Quart Rev Biol 63:265–289CrossRefPubMedGoogle Scholar
  8. Büschges A, Wolf H (1999) Phase-dependent presynaptic modulation of mechanosensory signals in the locust flight system. J Neurophysiol 81:959–962PubMedGoogle Scholar
  9. Camhi JM (1970) Yaw-correcting postural changes in locusts. J Exp Biol 52:519–531Google Scholar
  10. Camhi JM, Sumbre G, Wendler G (1995) Wing-beat coupling between flying locust pairs: preferred phase and lift enhancement. J Exp Biol 198:1051–1063PubMedGoogle Scholar
  11. Dawson JW, Dawson-Scully K, Robert D, Robertson RM (1997) Forewing asymmetries during auditory avoidance in flying locusts. J Exp Biol 200:2323–2335PubMedGoogle Scholar
  12. Dugard JJ (1967) Directional change in flying locusts. J Insect Physiol 13:1055–1063CrossRefGoogle Scholar
  13. Elson RC (1987) Integration of wing proprioceptive and descending exteroceptive sensory inputs by thoracic interneurons of the locust. J Exp Biol 128:193–217Google Scholar
  14. Gewecke M (1975) The influence of the air-current sense organs on the flight behaviour of Locusta migratoria. J Comp Physiol 103:79–95CrossRefGoogle Scholar
  15. Goodman LJ, Mobbs PG, Kirkham JB (1979) The fine structure of the ocelli of Schistocerca gregaria: the neuronal organisation of the synaptic plexus. Cell Tissue Res 196:487–510CrossRefPubMedGoogle Scholar
  16. Griss C, Rowell CHF (1986) Three descending interneurons reporting deviation from course in the locust. I. Anatomy. J Comp Physiol A 158:765–774CrossRefPubMedGoogle Scholar
  17. Gueron S, Levit-Gurevich K (1998) Computation of the internal forces in cilia: application to ciliary motion, the effects of viscosity, and cilia interactions. Biophys J 74:1658–1676CrossRefPubMedGoogle Scholar
  18. Horsmann U, Heinzel HG, Wendler G (1983) The phasic influence of self-generated air current modulations on the locust flight motor. J Comp Physiol 150:427–438CrossRefGoogle Scholar
  19. Kutsch W, Camhi J, Sumbre G (1994) Close encounters among flying locusts produce wing-beat coupling. J Comp Physiol A 174:643–649CrossRefPubMedGoogle Scholar
  20. Kutsch W, van der Wall M, Fischer H (1999) Analysis of free forward flight of Schistocerca gregaria employing telemetric transmission of muscle potentials. J Exp Zool 284:119–129CrossRefGoogle Scholar
  21. Medvedev GS, Wilson CJ, Callaway JC, Kopell N (2003) Dendritic synchrony and transient dynamics in a coupled oscillator model of the dopaminergic neuron. J Comput Neurosci 15:53–69CrossRefPubMedGoogle Scholar
  22. Michaels DC, Matyas EP, Jalife J (1987) Mechanism of sinoatrial pacemaker synchronisation: a new hypothesis. Circ Res 61:704–714PubMedGoogle Scholar
  23. Mizunami M (1994) Information processing in the insect ocellar system: comparative approaches to the evolution of visual processing and neural circuits. Adv Insect Physiol 25:151–265CrossRefGoogle Scholar
  24. Pfau HK, Nachtigall W (1981) Der Vorderflügel großer Heuschrecken als Luftkrafterzeuger. II: Zusammenspiel von Muskeln und Gelenkmechanik bei der Einstellung der Flügelgeometrie. J Comp Physiol A 142:135–140CrossRefGoogle Scholar
  25. Pikovsky A, Rosenblum M, Kurths J (2003) Synchronisation—a universal concept in nonlinear sciences. Cambridge University Press, CambridgeGoogle Scholar
  26. Reichert H, Rowell CHF (1985) Integration of nonphaselocked exteroceptive information in the control of rhythmic flight in the locust. J Neurophysiol 53:1201–1218PubMedGoogle Scholar
  27. Reye DN, Pearson KG (1988) Entrainment of the locust central flight oscillator by wing stretch receptor stimulation. J Comp Physiol A 162:77–89CrossRefGoogle Scholar
  28. Robertson RM, Reye DN (1992) Wing movements associated with collision-avoidance manoeuvres during flight in the locust Locusta migratoria. J Exp Biol 163:231–258Google Scholar
  29. Robertson RM, Kuhnert CT, Dawson JW (1996) Thermal avoidance during flight in the locust Locusta migratoria. J Exp Biol 199:1383–1393PubMedGoogle Scholar
  30. Rowell CHF, Pearson KG (1983) Ocellar input to the flight motor system of the locust: structure and function. J Exp Biol 103:265–288Google Scholar
  31. Rowell CHF, Reichert H (1986) Three descending interneurons reporting deviation from course in the locust. II. Physiology. J Comp Physiol A 158:775–794CrossRefPubMedGoogle Scholar
  32. Schmidt J, Zarnack W (1987) The motor pattern of locusts during visually induced rolling in long-term flight. Biol Cybern 56:397–410CrossRefGoogle Scholar
  33. Simmons PJ (1980) A locust wind and ocellar brain neurone. J Exp Biol 85:281–294Google Scholar
  34. Simmons PJ (1993) Adaptation and responses to changes in illumination by second- and third-order neurons of locust ocelli. J Comp Physiol A 173:635–648Google Scholar
  35. Simmons PJ (2002) Signal processing in a simple visual system: the locust ocellar system and its synapses. Microsc Res Tech 56:270–280CrossRefPubMedGoogle Scholar
  36. Simmons PJ, de Ruyter van Steveninck (2005) Reliability of signal transfer at a tonically transmitting, graded potential synapse of the locust ocellar pathway. J Neurosci 25:7529–7535Google Scholar
  37. Stange G (1981) The ocellar component of flight equilibrium control in dragonflies. J Comp Physiol 141:335–347CrossRefGoogle Scholar
  38. Taylor CP (1981) Contribution of compound eyes and ocelli to steering of locusts in flight. J Exp Biol 93:1–18Google Scholar
  39. Taylor GK, Thomas ALR (2003) Dynamic flight stability in the desert locust Schistocerca gregaria. J Exp Biol 206:2803–2829CrossRefPubMedGoogle Scholar
  40. Waldmann B, Zarnack W (1988) Forewing movements and motor activity during roll manoeuvers in flying desert locusts. Biol Cybern 59:325–335CrossRefGoogle Scholar
  41. Waldron I (1967) Neural mechanism by which controlling inputs influence motor output in the flying locust. J Exp Biol 47:213–228PubMedGoogle Scholar
  42. Waldron I (1968) The mechanism of coupling of the locust flight oscillator to oscillatory inputs. Z Vgl Physiol 57:331–347CrossRefGoogle Scholar
  43. Weis-Fogh T, Jensen M (1956) Biology and physics of locust flight. I. Basic principles in insect flight. A critical review. Philos Trans R Soc London B 239:415–458CrossRefGoogle Scholar
  44. Wendler G (1974) The influence of proprioceptive feedback on locust flight coordination. J Comp Physiol 88:173–200CrossRefGoogle Scholar
  45. Wilson M (1978) The functional organisation of locust ocelli. J Comp Physiol 124:297–316CrossRefGoogle Scholar
  46. Wolf H (1993) The locust tegula: significance for flight rhythm generation, wing movement control and aerodynamic force production. J Exp Biol 182:229–253Google Scholar
  47. Wolf H, Pearson KG (1988) Proprioceptive input patterns flight elevator activity in the locust flight system. J Neurophysiol 59:1831–1853PubMedGoogle Scholar
  48. Zarnack W (1972) Flugbiophysik der Wanderheuschrecke (Locusta migratoria L.). I. Die Bewegungen der Vorderflügel. J Comp Physiol 78:356–395CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  1. 1.Department of Biology, Animal PhysiologyPhilipps-University of MarburgMarburgGermany
  2. 2.Visual Sciences, Research School of Biological SciencesAustralian National UniversityCanberraAustralia

Personalised recommendations