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A neural basis for gyroscopic force measurement in the halteres of Holorusia

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Abstract

Dipteran flight requires rapid acquisition of mechanosensory information provided by modified hindwings known as halteres. Halteres experience torques resulting from Coriolis forces that arise during body rotations. Although biomechanical and behavioral data indicate that halteres detect Coriolis forces, there are scant data regarding neural encoding of these or any other forces. Coriolis forces arise on the haltere as it oscillates in one plane while rotating in another, and occur at oscillation frequency and twice the oscillation frequency. Using single-fiber recordings of haltere primary afferent responses to mechanical stimuli, we show that spike rate increases linearly with stimulation frequency up to 150 Hz, much higher than twice the natural oscillation frequency of 40 Hz. Furthermore, spike-timing precision is extremely high throughout the frequency range tested. These characteristics indicate that afferents respond with high speed and high precision, neural features that are useful for detecting Coriolis forces. Additionally, we found that neurons respond preferentially to specific stimulus directions, with most responding more strongly to stimulation in the orthogonal plane. Directional sensitivity, coupled with precise, high-speed encoding, suggests that haltere afferents are capable of providing information about forces occurring at the haltere base, including Coriolis forces.

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Acknowledgments

We thank Wai Pang Chan for helpful comments and imaging assistance, Alexandre Dieudonné for advice on experiments, and Doug Ewing and the Nielsen family for crane fly collection. We also thank Michael Dickinson for valuable commentary on the manuscript. All experiments complied with the “Principles of animal care”, publication no. 86–23, revised 1985 of the National Institute of Health. Support was provided by the Komen Endowed Chair and a grant from the Air Force Office of Scientific Research to TLD.

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  1. Department of Biology, Program in Neurobiology and Behavior, University of Washington, Seattle, WA, 98195, USA

    J. L. Fox & T. L. Daniel

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  1. J. L. Fox
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  2. T. L. Daniel
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Correspondence to J. L. Fox.

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Fox, J.L., Daniel, T.L. A neural basis for gyroscopic force measurement in the halteres of Holorusia . J Comp Physiol A 194, 887–897 (2008). https://doi.org/10.1007/s00359-008-0361-z

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  • DOI: https://doi.org/10.1007/s00359-008-0361-z

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