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Encoding noxious heat by spike bursts of antennal bimodal hygroreceptor (dry) neurons in the carabid Pterostichus oblongopunctatus

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Abstract

Despite thermosensation being crucial in effective thermoregulation behaviour, it is poorly studied in insects. Very little is known about encoding of noxious high temperatures by peripheral thermoreceptor neurons. In carabids, thermo- and hygrosensitive neurons innervate antennal dome-shaped sensilla (DSS). In this study, we demonstrate that several essential fine structural features of dendritic outer segments of the sensory neurons in the DSS and the classical model of insect thermo- and hygrosensitive sensilla differ fundamentally. Here, we show that spike bursts produced by the bimodal dry neurons in the antennal DSS may contribute to the sensation of noxious heat in P. oblongopunctatus. Our electrophysiological experiments showed that, at temperatures above 25 °C, these neurons switch from humidity-dependent regular spiking to temperature-dependent spike bursting. Five out of seven measured parameters of the bursty spike trains, the percentage of bursty dry neurons, the CV of ISIs in a spike train, the percentage of bursty spikes, the number of spikes in a burst and the ISIs in a burst, are unambiguously dependent on temperature and thus may precisely encode both noxious high steady temperatures up to 45 °C as well as rapid step-changes in it. The cold neuron starts to produce temperature-dependent spike bursts at temperatures above 30–35 °C. Thus, the two neurons encode different but largely overlapping ranges in noxious heat. The extent of dendritic branching and lamellation of the neurons largely varies in different DSS, which might be the structural basis for their variation in threshold temperatures for spike bursting.

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Acknowledgments

The study was supported by institutional research funding IUT36-2 of the Estonian Ministry of Education and Research and Estonian State Forest Management forest protection project (2012–2015) (T12115MIMK).

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Authors and Affiliations

  1. Institute of Agricultural and Environmental Sciences, Estonian University of Life Sciences, Kreutzwaldi Street 1, 51014, Tartu, Estonia

    Anne Must, Enno Merivee, Karin Nurme, Ingrid Williams & Ene Tooming

  2. Institute of Forestry and Rural Engineering, Estonian University of Life Sciences, Kreutzwaldi Street 1, 51014, Tartu, Estonia

    Ivar Sibul

  3. Department of Science, University of Roma Tre, Viale G. Marconi 446, I-00146, Rome, Italy

    Maurizio Muzzi & Andrea Di Giulio

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  1. Anne Must
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Must, A., Merivee, E., Nurme, K. et al. Encoding noxious heat by spike bursts of antennal bimodal hygroreceptor (dry) neurons in the carabid Pterostichus oblongopunctatus . Cell Tissue Res 368, 29–46 (2017). https://doi.org/10.1007/s00441-016-2547-y

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