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Identification of the origin of force-feedback signals influencing motor neurons of the thoraco-coxal joint in an insect

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Abstract

Force feedback from Campaniform sensilla (CS) on insect limbs helps to adapt motor outputs to environmental conditions, but we are only beginning to reveal the neural control mechanisms that mediate these influences. We studied CS groups that affect control of the thoraco-coxal joint in the stick insect Carausius morosus by applying horizontal and vertical forces to the leg stump. Motor effects of ablation of CS groups were evaluated by recording extracellularly from protractor (ProCx) and retractor (RetCx) nerves. Extracellular recordings showed that the effects of stimulating the sensilla were consistent with their broad ranges of directional sensitivity: for example, RetCx firing in response to posterior bending could be reduced by ablating several groups of trochanteral CS, whereas ablation of tibial and femoral sensilla had little effect. In contrast, ProCx motor neuron activity upon anteriorly directed stimuli was affected mainly by ablating a single CS group (G2). Dye fills of trochanteral, femoral and tibial CS groups with fluorescent dyes revealed a common projection pattern with little group specificity. These findings support the idea that the influences of CS feedback are determined by the activities of pre-motor interneurons, facilitating fast and task-dependent adaptation to changing environmental conditions.

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Abbreviations

abl.:

Ablated

C. morosus :

Carausius morosus

CS:

Campaniform sensilla

CTr:

Coxo-trochanteral

FTi:

Femur–tibial

ncr:

Nervus cruris

ThC:

Thorax–coxal

ProCx:

Protractor coxae

RetCx:

Retractor coxae

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Acknowledgements

We sincerely thank H.-P. Bollhagen for excellent technical assistance at the scanning electron microscope, S. Seyed-Nejadi, S. Seeliger, and M. Dübbert for providing laboratory and technical support, and Ch. Mantziaris for helpful advice and inspiring discussions. We also thank the Imaging Facility of the Cologne Biocenter for support of our study. Finally, we thank the two anonymous reviewers for their constructive criticism that helped us to improve the manuscript. We confirm that all animals were kept and handled according to the pertinent guidelines. This study was supported by DFG Bu 857/14.

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  1. Department for Animal Physiology, Institute for Zoology, Biocenter Cologne, University of Cologne, Zülpicher Strasse 47b, 50674, Cologne, Germany

    Anna Haberkorn, Matthias Gruhn, Sasha N. Zill & Ansgar Büschges

  2. Department of Biomedical Sciences, Joan C. Edwards School of Medicine, Marshall University, Huntington, WV, 25704, USA

    Sasha N. Zill

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  1. Anna Haberkorn
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Haberkorn, A., Gruhn, M., Zill, S.N. et al. Identification of the origin of force-feedback signals influencing motor neurons of the thoraco-coxal joint in an insect. J Comp Physiol A 205, 253–270 (2019). https://doi.org/10.1007/s00359-019-01334-4

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