Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Complex auditory behaviour emerges from simple reactive steering

Abstract

The recognition and localization of sound signals is fundamental to acoustic communication1,2. Complex neural mechanisms are thought to underlie the processing of species-specific sound patterns even in animals with simple auditory pathways3,4. In female crickets, which orient towards the male's calling song, current models propose pattern recognition mechanisms based on the temporal structure of the song5,6,7. Furthermore, it is thought that localization is achieved by comparing the output of the left and right recognition networks, which then directs the female to the pattern that most closely resembles the species-specific song8,9,10. Here we show, using a highly sensitive method for measuring the movements of female crickets, that when walking and flying each sound pulse of the communication signal releases a rapid steering response. Thus auditory orientation emerges from reactive motor responses to individual sound pulses. Although the reactive motor responses are not based on the song structure, a pattern recognition process may modulate the gain of the responses on a longer timescale. These findings are relevant to concepts of insect auditory behaviour and to the development of biologically inspired robots performing cricket-like auditory orientation11,12,13.

Your institute does not have access to this article

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 1: Trackball system for testing auditory orientation of crickets.
Figure 2: Cricket orientation to songs that are split between two speakers.
Figure 3: Cricket orientation to randomly split songs with different numbers of pulses presented from each side.
Figure 4: Cricket orientation to patterns of different attractiveness.

References

  1. Webster, D. B., Fay, R. R. & Popper, A. N. The Evolutionary Biology of Hearing (Springer, Berlin, New York, 1992)

    Book  Google Scholar 

  2. Pollack, G. S. Analysis of temporal patterns of communication signals. Curr. Opin. Neurobiol. 11, 734–738 (2001)

    CAS  Article  Google Scholar 

  3. Balakrishnan, R., von Helversen, D. & von Helversen, O. Song pattern recognition in the grasshopper Chorthippus biguttulus: the mechanism of syllable onset and offset detection. J. Comp. Physiol. A 187, 255–264 (2001)

    CAS  Article  Google Scholar 

  4. Weber, T. & Thorson, J. in Cricket Behaviour and Neurobiology (eds Huber, F., Moore, T. E. & Loher, W.) 310–339 (Cornell Univ. Press, Ithaca, London, 1989)

    Google Scholar 

  5. Hoy, R. R. Acoustic communication in crickets: a model system of feature detection. Fed. Proc. 37, 2316–2323 (1978)

    CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  7. Hennig, R. M. Acoustic feature extraction by cross correlation in crickets? J. Comp. Physiol. A 189, 589–598 (2003)

    ADS  CAS  Article  Google Scholar 

  8. Pollack, G. S. Discrimination of calling song models by the cricket, Teleogryllus oceanicus: the influence of sound direction on neural encoding of the stimulus temporal pattern and on phonotactic behaviour. J. Comp. Physiol. A 158, 549–561 (1986)

    Article  Google Scholar 

  9. Stabel, J., Wendler, G. & Scharstein, H. Cricket phonotaxis: localization depends on recognition of the calling song pattern. J. Comp. Physiol. A 165, 165–177 (1989)

    Article  Google Scholar 

  10. von Helversen, D. & von Helversen, O. Acoustic pattern recognition and orientation in orthopteran insects: parallel or serial processing? J. Comp. Physiol. A 177, 767–774 (1995)

    Article  Google Scholar 

  11. Webb, B. Robots in invertebrate neuroscience. Nature 417, 359–363 (2002)

    ADS  CAS  Article  Google Scholar 

  12. Webb, B. & Scutt, T. A simple latency-dependent spiking-neuron model of cricket phonotaxis. Biol. Cybern. 82, 247–269 (2000)

    CAS  Article  Google Scholar 

  13. Arkin, R. C. Behaviour-Based Robotics (MIT, Cambridge, London, 1998)

    Google Scholar 

  14. Gerhard, H. C. & Huber, F. Acoustic Communication in Insects and Anurans (Univ. of Chicago Press, Chicago and London, 2002)

    Google Scholar 

  15. Huber, F. Cricket neuroethology: neuronal basis of intraspecific acoustic communication. Adv. Study Behav. 19, 299–356 (1990)

    Article  Google Scholar 

  16. Pollack, G. S. Who, what, where? Recognition and localization of acoustic signals by insects. Curr. Opin. Neurobiol. 10, 763–767 (2000)

    CAS  Article  Google Scholar 

  17. Popov, A. V. & Shuvalov, V. F. Phonotactic behaviour of crickets. J. Comp. Physiol. A 119, 111–126 (1977)

    Article  Google Scholar 

  18. Doherty, J. A. Temperature coupling and trade-off phenomena in the acoustic communication system of the cricket, Gryllus bimaculatus de Geer (Gryllidae). J. Exp. Biol. 114, 17–35 (1985)

    Google Scholar 

  19. Murphey, R. K. & Zaretsky, M. D. Orientation to calling song by female crickets, Scasipedus marginatus (Gryllidae). J. Exp. Biol. 56, 335–352 (1972)

    CAS  PubMed  Google Scholar 

  20. Ulagarai, S. M. & Walker, T. J. Phonotaxis of crickets in flight: attraction of male and female crickets to male calling songs. Science 182, 1278–1279 (1973)

    ADS  Article  Google Scholar 

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

    ADS  CAS  Article  Google Scholar 

  22. Schildberger, K., Huber, F. & Wohlers, D. W. in Cricket Behaviour and Neurobiology (eds Huber, F., Moore, T. E. & Loher, W.) 423–458 (Cornell Univ. Press, Ithaca, London, 1989)

    Google Scholar 

  23. Weber, T., Thorson, J. & Huber, F. Auditory behaviour of the cricket. I: Dynamics of compensated walking and discrimination paradigms on the Kramer treadmill. J. Comp. Physiol. A 141, 215–232 (1981)

    Article  Google Scholar 

  24. Schmitz, B., Scharstein, H. & Wendler, G. Phonotaxis in Gryllus campestris L. (Orthoptera, Gryllidae). I: Mechanism of acoustic orientation in intact female crickets. J. Comp. Physiol. A 148, 431–444 (1982)

    Article  Google Scholar 

  25. Doherty, J. A. Song recognition and localization in the phonotaxis behavior of the field cricket, Gryllus bimaculatus (Orthoptera: Gryllidae). J. Comp. Physiol. A 168, 213–222 (1991)

    Article  Google Scholar 

  26. Weber, T. & Thorson, J. Auditory behaviour of the cricket. IV: Interaction of direction of tracking with perceived split-song paradigms. J. Comp. Physiol. A 163, 13–22 (1988)

    Article  Google Scholar 

  27. Hedwig, B. A highly sensitive opto-electronic system for the measurement of movements. J. Neurosci. Methods 100, 165–171 (2000)

    CAS  Article  Google Scholar 

  28. Pollack, G. S. & Hoy, R. R. Phonotaxis in flying crickets: neural correlates. J. Insect Physiol. 27, 41–45 (1981)

    Article  Google Scholar 

  29. Nabatiyan, A., Poulet, J. F. A., de Polavieja, G. G. & Hedwig, B. Temporal pattern recognition based on instantaneous spike rate coding in a simple auditory system. J. Neurophysiol. 90, 2484–2493 (2003)

    CAS  Article  Google Scholar 

  30. Cade, W. H. Effect of male deprivation on female phonotaxis in field crickets (Orthoptera: Gryllidae; Gryllus). Can. Entomol. 111, 741–744 (1979)

    Article  Google Scholar 

Download references

Acknowledgements

We thank our Cambridge and Edinburgh colleagues for comments on the manuscript. The BBSRC and the Royal Society supported the project. We are grateful to M. Knepper and P. Williams for the development of software and hardware and to Röhm GmbH for providing Rohacell.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Berthold Hedwig or James F. A. Poulet.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Hedwig, B., Poulet, J. Complex auditory behaviour emerges from simple reactive steering. Nature 430, 781–785 (2004). https://doi.org/10.1038/nature02787

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature02787

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing