Skip to main content
SpringerLink
Log in

Auditory interneurons in locusts produce directional head and abdomen movements

  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Summary

Locusts (Locusta migratoria) were stimulated with pulses of pure tones of frequencies between 5 kHz and 25 kHz. Interneurons responding to these stimuli (auditory interneurons) were recorded intracellularly and identified by dye injection. Their output functions were investigated by injection of depolarizing current during simultaneous registration of components of flight steering behavior of the animals, i.e. movements of the head and the abdomen and flight activity. Three different types of effects were found, corresponding to 3 functional classes of interneurons:

  1. (1)

    Auditory interneurons in the metathoracic ganglion can activate (Fig. 1) or inhibit (Fig. 2) the flight oscillator when depolarized.

  2. (2)

    Resting tethered locusts can perform lateral bending of the abdomen and, less prominent, head turns towards the sound source at frequencies between 5 and 15 kHz and at high intensities (70 dB and up, Fig. 3). Auditory interneurons were found which are sensitive to sound pulses with frequencies of 5 kHz to 15 kHz and some of them are directional (Fig. 4). Injection of depolarizing current into these cells causes movements of head and abdomen to the same side (Figs. 6, 7).

  3. (3)

    A third population of metathoracic and abdominal interneurons is also excited by pure tone pulses (Figs. 9, 11, 12). Current injected into these cells, and into a descending auditory interneuron (Fig. 8) results in spike activity, driving the head and the abdomen in opposite directions. These movements are components of the characteristic steering behavior seen in the negatively phonotactic response to pulsed ultrasound of intact tethered animals, which is thought to be involved in bat avoidance (Robert 1989).

The frequency responses of the interneurons and their output effects are discussed in the context of two basically different behaviors: a positive phonotaxis, which might be used during intraspecific communication, and an avoidance steering behavior to escape hunting bats.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

DN :

Descending neuron

AG2 :

Abdominal neuromere 2

T3 :

Metathoracic neuromere

MVT :

Median ventral tract

DIT :

Dorsal intermediate tract

References

  • Adam L-J (1969) Neurophysiologie des Hörens und Bioakustik einer Feldheuschrecke (Locusta migratoria). Z Vergl Physiol 63:227–289

    Google Scholar 

  • Altman JS, Kien J (1988) A model for decision-making in the insect nervous system. In: Ali MA (ed) Nervous systems in invertebrates. Plenum Publ Corp, New York, pp 621–643

    Google Scholar 

  • Baader A (1990a) The posture of the abdomen during locust flight: regulation by steering and ventilatory interneurones. J Exp Biol 151:109–131

    Google Scholar 

  • Baader A (1990b) An ascending visual pathway in locusts. Naturwissenschaften 77:338–340

    Google Scholar 

  • Baader A (1991) Simulation of self-motion in tethered flying insects: an optical flow field for locusts. J Neurosci Methods, in press

  • Boyan GS (1985) Auditory input to the flight system of the locust. J Comp Physiol A 156:79–91

    Google Scholar 

  • Boyan GS, Fullard JH (1986) Interneurones responding to sound in the tobacco budworm moth Heliothis virescens (Noctuidae): morphological and physiological characteristics. J Comp Physiol A 158:391–404

    Google Scholar 

  • Brodfuehrer PD, Hoy RR (1989) Integration of ultrasound and flight inputs on descending neurons in the cricket brain. J Exp Biol 145:157–171

    Google Scholar 

  • Camhi JM (1970) Yaw-correcting postural changes in locusts. J Exp Biol 52:519–531

    Google Scholar 

  • Dugard JJ (1967) Directional change in flying locusts. J Insect Physiol 13:1055–1063

    Google Scholar 

  • Gewecke M, Philippen J (1978) Control of the horizontal flightcourse by air current sense organs in Locusta migratoria. Physiol Entomol 3:43–52

    Google Scholar 

  • Griffin DR (1958) Listening in the dark. Yale Univ Press, New Haven

    Google Scholar 

  • Haskell PT (1957) The influence of flight noise on behavior in the desert locust, Schistocerca gregaria. J Insect Physiol 1:52–75

    Google Scholar 

  • Hedwig B (1985) Untersuchungen zur Kontrolle des Feldheuschreckengesangs durch intersegmentale Neurone. PhD Thesis, University of Göttingen, FRG

    Google Scholar 

  • Hedwig B (1986) On the role in stridulation of plurisegmental interneurons of the acridid grasshopper Omocestus viridulus L. II. Anatomy and physiology of ascending and T-shaped interneurons. J Comp Physiol A 158:429–444

    Google Scholar 

  • Helversen D von, Rheinlaender J (1988) Interaural intensity and time discrimination in an unrestraint grasshopper: a tentative behavioural approach. J Comp Physiol A 162:333–340

    Google Scholar 

  • Hensler K (1985) Neuronale Steuerung während des Augenputzverhaltens von Grillen. PhD Thesis, University of Konstanz, FRG

    Google Scholar 

  • Hoy RR (1989) Startle, categorical response, and attention in acoustic behavior of insects. Annu Rev Neurosci 12:355–375

    Google Scholar 

  • Kalmring K (1975) The afferent auditory pathway in the ventral nerve cord of Locusta migratoria (Acrididae). I. Synaptic con-nectivity and information processing among the auditory neu rons of the ventral cord. J Comp Physiol 104:103–141

    Google Scholar 

  • Kalmring K, Eisner N (eds) (1985) Acoustic and vibrational communication in insects. Paul Parey, Berlin Hamburg

    Google Scholar 

  • Kick SA (1982) Target-detection by the echolocating bat, Eptesicus fuscus. J Comp Physiol 145:431–435

    Google Scholar 

  • Kupfermann I, Weiss KR (1978) The command neuron concept. Behav Brain Sci 1:3–39

    Google Scholar 

  • Madsen BM, Miller LA (1987) Auditory input to motor neurons of the dorsal longitudinal flight muscles in a noctuid moth (Barathra brassicae L.). J Comp Physiol A 160:23–31

    Google Scholar 

  • Marquart V (1985 a) Auditorische Interneurone im thorakalen Nervensystem von Heuschrecken: Morphologie, Physiologie und synaptische Verbindungen. PhD Thesis, University of Bochum, FRG

    Google Scholar 

  • Marquart V (1985b) Local interneurons mediating excitation and inhibition onto ascending neurons in the auditory pathway of grasshoppers. Naturwissenchaften 72:42–44

    Google Scholar 

  • May ML, Hoy RR (1990) Ultrasound-induced yaw movements in the flying Australian field cricket (Teleogryllus oceanicus). J Exp Biol 149:177–189

    Google Scholar 

  • Michelsen A (1971) The physiology of the locust ear. I. Frequency sensitivity of single cells in the isolated ear. J Comp Physiol 71:49–62

    Google Scholar 

  • Michelsen A (1983) The biophysical basis of sound communication. In: Lewis B (ed) Bioacoustics: a comparative approach. Academic Press, London, pp 3–38

    Google Scholar 

  • Miller LA, Olesen J (1979) Avoidance behavior in green lacewings. J Comp Physiol 131:113–120

    Google Scholar 

  • Moiseff A, Hoy RR (1983) Sensitivity to ultrasound in an identified auditory interneuron in the cricket: a possible neural link to phonotactic behavior. J Comp Physiol 152:155–167

    Google Scholar 

  • Moiseff A, Pollack GS, Hoy RR (1978) Steering responses of flying crickets to sound and ultrasound: mate attraction and predator avoidance. Proc Natl Acad Sci USA 75:4052–4056

    Google Scholar 

  • Nolen TG, Hoy RR (1984) Initiation of behavior by single neurons: the role of behavioral context. Science 226:992–994

    Google Scholar 

  • Nolen TG, Hoy RR (1986a) Phonotaxis in flying crickets. I. Attraction to the calling song and avoidance of bat-like ultrasound are discrete behaviors. J Comp Physiol A 159:423–439

    Google Scholar 

  • Nolen TG, Hoy RR (1986b) Phonotaxis in flying crickets. II. Physiological mechanisms of two-tone suppression of the high frequency avoidance steering behavior by the calling song. J Comp Physiol A 159:441–456

    Google Scholar 

  • Popov AV, Shuvalov VF (1977) Phonotactic behavior of crickets.J Comp Physiol 119:111–126

    Google Scholar 

  • Ramirez J-M, Pearson KG (1988) Generation of motor patterns for walking and flight in motoneurons supplying bifunctional muscles in the locust. J Neurobiol 19:257–282

    Google Scholar 

  • Regen J (1924) Über die Orientierung des Weibchens von Liogrillus campestris L. tnach dem Stridulationsschall des Männchens. Akad Wiss Wien Math Naturwiss Kl 132:81–88

    Google Scholar 

  • Rehbein HG (1976) Auditory neurons in the ventral cord of the locust: morphological and functional properties. J Comp Physiol 110:233–250

    Google Scholar 

  • Rehbein H, Kalmring K, Römer H (1974) Structure and function of acoustic neurons in the thoracic ventral nerve cord of Locusta migratoria (Acrididae). J Comp Physiol 95:263–280

    Google Scholar 

  • Reichert H, Rowell CHF (1985) Integration of nonphaselocked exteroceptive information in the control of rhythmic flight in the locust. J Neurophysiol 53:1202–1218

    Google Scholar 

  • Robert D (1989) The auditory behaviour of flying locusts. J Exp Biol 147:279–301

    Google Scholar 

  • Robertson RM, Pearson KG (1983) Interneurons in the flight system of the locust: distribution, connections and resetting properties. J Comp Neurol 215:3–50

    Google Scholar 

  • Roeder KD (1967) Turning tendency of moths exposed to ultrasound while in stationary flight. J Insect Physiol 13:873–888

    Google Scholar 

  • Roeder KD (1969) Acoustic interneurons in the brain of noctuid moths. J Insect Physiol 15:1713–1718

    Google Scholar 

  • Römer H, Marquart V (1984) Morphology and physiology of auditory interneurons in the metathoracic ganglion of the locust. J Comp Physiol A 155:249–262

    Google Scholar 

  • Römer H, Scikowski U (1985) Responses to model songs of auditory neurons in the thoracic ganglia and brain of the locust. J Comp Physiol A 156:845–860

    Google Scholar 

  • Römer H, Marquart V, Hardt M (1988) Organization of a sensory neuropile in the auditory pathway of two groups of Orthoptera. J Comp Neurol 275:201–215

    Google Scholar 

  • Rowell CHF (1989) Descending interneurones of the locust reporting deviation from flight course: what is their role in steering? J Exp Biol 146:177–194

    Google Scholar 

  • Sandeman DC (1968) A sensitive position measuring device for biological systems. Comp Biochem Physiol 24:635–638

    Google Scholar 

  • Schildberger K (1984) Temporal selectivity of identified auditory neurons in the cricket brain. J Comp Physiol A 155:171–185

    Google Scholar 

  • Stewart WW (1978) Functional connections between cells as revealed by dyecoupling with a highly fluorescent naphthalimide tracer. Cell 14:741–759

    Google Scholar 

  • Tyrer NM, Gregory GE (1982) A guide to the neuroanatomy of locust suboesophageal and thoracic ganglia. Phil Trans R Soc London Ser B 297:91–123

    Google Scholar 

  • Wohlers DW, Huber F (1982) Processing of sound signals by six types of neurons in the prothoracic ganglion of the cricket, Gryllus bimaculatus L. J Comp Physiol 146:161–173

    Google Scholar 

  • Ulagaraj SM, Walker TJ (1973) Phonotaxis of crickets in flight: attraction of male and female crickets to male calling songs. Science 182:1278–1279

    Google Scholar 

  • Yager DD, Hoy RR (1986) The cyclopean ear: a new sense organ for the praying mantis. Science 231:727–729

    Google Scholar 

  • Yinon U, Shulov A, Tsvilich R (1971) Audition in the desert locust: behavioural and neurophysiological studies. J Exp Biol 55:713–725

    Google Scholar 

Download references

Author information

Author notes

  1. Andreas Baader

    Present address: Department of Biology, B-022 University of California, 92093, San Diego, La Jolla, CA, USA

Authors and Affiliations

  1. Zoologisches Institut der Universität Basel, Rheinsprung 9, CH-4051, Basel, Switzerland

    Andreas Baader

Authors
  1. Andreas Baader
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Baader, A. Auditory interneurons in locusts produce directional head and abdomen movements. J Comp Physiol A 169, 87–100 (1991). https://doi.org/10.1007/BF00198175

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00198175

Key words

Search

Navigation