Summary
Locusts, Locusta migratoria, flying under closed-loop conditions in a flight simulator, control the stability of their visual environment by means of correctional steering and so minimize retinal slip (the optomotor reaction). Correctional steering includes modulation of the wingbeat, ruddering with abdomen and legs and compensatory head movements. Pulsed ultrasounds that simulate bat echolocation signals elicit avoidance steering in flying locusts: ruddering and yaw torque are directed away from the sound source. In this article the two modes of steering are compared and their interaction is studied.
-
1.
In both correctional and avoidance steering ruddering is directed to the side of the turn. However, during correctional manoeuvres, head movements are also directed to the side of the turn, while during avoidance steering the head moves in the direction opposite to that of the turn (Fig. 4).
-
2.
The components and temporal organization of both sorts of steering are similar. Head movements occur some 30–40 ms after torque production begins (Fig. 5). Thus, neither correctional nor avoidance steering is initiated by head movements.
-
3.
Under closed-loop conditions, avoidance steering generates pronounced rotation of the panorama (Figs. 6, 7) that is not counteracted by the compensatory optomotor reflex.
-
4.
Acoustically elicited head turns are also performed in darkness (Fig. 4a), and irrespective of the sign of the visual reafference (Fig. 9), which indicates that they are temporarily independent of visual information. A mechanism is proposed in which optomotor interference is prevented by an inhibitory corollary discharge of acoustic origin.
-
5.
Locusts prevented from moving their heads still perform avoidance turns (Fig. 8), but these are of shorter duration than when the head is free.
-
6.
The role of head movements in steering is discussed. It is proposed that neck proprioception assists visual and acoustic information in adaptive flight steering. Head movements in closed-loop corrective steering reduce steering overshoot; during avoidance steering opposite head movements may in turn favor steering overshoot.
Similar content being viewed by others
References
Arbas EA (1986) Control of hindlimb posture by wind-sensitive hairs and antennae during locust flight. J Comp Physiol A 159:849–885
Bell CC (1981) An efference copy which is modified by reafferent input. Science 214:450–453
Camhi JM (1970) Yaw-correcting postural changes in locusts. J Exp Biol 52:519–531
Camhi JM (1984) Neuroethology. Nerve cells and the natural behavior of animals. Sinauer Assoc Inc, Sunderland, Mass., pp 344–345
Collett TS (1980) Angular tracking and the optomotor response. An analysis of visual reflex interaction in a hoverfly. J Comp Physiol 140:145–158
Copp NH, Watson D (1988) Visual control of turning responses to tactile stimuli in the crayfish Procambarus clarkii. J Comp Physiol A 163:175–186
Dugard JJ (1967) Directional change in flying locusts. J Insect Physiol 13:1055–1063
Forman R, Brumbley D (1980) An improved capacitive position transducer for biological systems. J Exp Biol 88:399–402
Geiger G, Poggio T (1977) On head and body movements of flying flies. Biol Cybern 25:177–180
Gewecke M, Philippen J (1978) Control of the horizontal flight course by air-current sense organs in Locusta migratoria. Physiol Entomol 3:43–52
Goodman LJ (1965) The role of certain optomotor reactions in regulating stability in the rolling plane during flight in the desert locust, Schistocerca gregaria. J Exp Biol 42:385–407
Götz KG (1987) Course-control, metabolism and wing interference during ultralong tethered flight in Drosophila melanogaster. J Exp Biol 128:35–46
Heisenberg M, Wolf R (1979) On the fine structure of yaw torque in visual flight orientation of Drosophila melanogaster. J Comp Physiol 130:113–130
Heisenberg M, Wolf R (1988) Reafferent control of optomotor yaw torque in Drosophila melanogaster. J Comp Physiol A 163:373–388
Hengstenberg R (1988) Mechanosensory control of compensatory head roll during flight in the blowfly Calliphora erythrocephala Meig. J Comp Physiol A 163:151–165
Hensler K (1988) The pars intercerebralis neurone PI(2)5 of locusts: convergent processing of inputs reporting head movements and deviations from straight flight. J Exp Biol 140:511–533
Hensler K, Robert D (1990) Compensatory head rolling during corrective flight steering in locusts. J Comp Physiol A 166:685–693
Holst E von, Mittelstaedt H (1950) Das Reafferenzprinzip (Wechselwirkung zwischen Zentralnervensystem und Peripherie). Naturwissenschaften 37:464–476
Land MF (1971) Orientation in jumping spider in the absence of visual feedback. J Exp Biol 54:119–139
Land MF (1975) Head movements and fly vision. In: Horridge A (ed) The compound eye and vision of insects. Clarendon Press, Oxford, pp 469–489
Miall RC (1989) A systems analysis of the role of head position during steering in locust flight. In: Erber J, Menzel R, Pflüger H-J, Todt D (eds) Neural mechanisms of behavior. Proc 2nd Internat Congr Neuroethology. Thieme, Stuttgart New York, Abstr 2
Miall RC (1990) Visual control of steering in locusts: the effects of head movement on responses to roll stimuli. J Comp Physiol A 166:735–744
Michelsen A (1971) The physiology of the locust ear. III. Acoustical properties of the intact ear. Z Vergl Physiol 71:102–128
Miller LA (1977) Directional hearing in the locust Schistocerca gregaria Forskål (Acrididae, Orthoptera). J Comp Physiol 119:85–98
Mittelstaedt H (1951) Zur Analyse physiologischer Regelungssysteme. Verh Dtsch Zool Ges, Zool Anz (Suppl): 150–157
Moiseff A, Pollack G, Hoy RR (1979) Steering responses of flying crickets to sound and ultrasound: mate attraction and predator avoidance. Proc Natl Acad Sci USA 75:4052–4056
Richmond BJ, Wurtz RH (1980) Vision during saccadic eye movements. II. A corollary discharge to monkey superior colliculus. J Neurophysiol 43:1156–1167
Robert D (1988) Visual steering under closed-loop conditions by flying locusts: flexibility of optomotor response and mechanisms of correctional steering. J Comp Physiol A 164:15–24
Robert D (1989) The auditory behaviour of flying locusts. J Exp Biol 147:279–301
Robert D, Rowell CHF (1992) Locust flight steering. I. Head movements and the organization of correctional manoeuvres. J Comp Physiol A 171:41–51
Rowell CHF (1989) Descending interneurones reporting deviation from flight course: what is their role in steering? J Exp Biol 146:177–194
Sandeman DC (1980) Angular acceleration, compensatory head movements and the halteres of flies (Lucilia serricata). J Comp Physiol 136:361–367
Sandeman DC, Markl H (1980) Head movements in flies (Calliphora) produced by deflection of the halteres. J Exp Biol 85:43–60
Schmidt J, Zarnack W (1987) The motor pattern of locusts during visually induced rolling in long-term flight. Biol Cybern 56:397–410
Taylor CP (1981a) Contribution of compound eyes and ocelli to steering of locusts in flight. I. Behavioural analysis. J Exp Biol 93:1–18
Taylor CP (1981b) Contribution of compound eyes and ocelli to steering of locusts in flight. II. Timing changes in flight motor units. J Exp Biol 93:19–31
Thüring DA (1986) Variability of the motor output during flight steering in locusts. J Comp Physiol A 156:655–664
Zaretsky M (1982) Quantitative measurements of centrally and retinally generated saccadic suppression in a locust movement detector neurone. J Physiol (Lond) 328:521–533
Zaretsky M, Rowell CHF (1979) Saccadic suppression by corollary discharge in the locust. Nature 280:583–585
Zarnack W, Möhl B (1977) Activity of the direct downstroke flight muscles of Locusta migratoria (L.) during steering behaviour in flight. I. Patterns of time shift. J Comp Physiol 118:215–233
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Robert, D., Rowell, C.H.F. Locust flight steering. J Comp Physiol A 171, 53–62 (1992). https://doi.org/10.1007/BF00195960
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00195960