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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.

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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.

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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.

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

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

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