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

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.

Neural Code for Ambient Heat Detection in Elaterid Beetles

“…Heat stress also has deleterious effects on insect metabolism, respiration, endocrine, and nervous systems, behavior, oviposition, development, and growth (Denlinger and Yocum, 1998;Chown and Terblanche, 2007). Research activity on various effects of temperature on ectothermic organisms has increased recently (Huey et al, 2012;Gilbert et al, 2014;Sunday et al, 2014;Abram et al, 2017;DeLong et al, 2017;Must et al, 2017;Nurme et al, 2018). In part, this has been motivated by the need to understand how individual organisms and ecosystems respond to ongoing global warming when high-temperature trends and daily extremes could become more commonplace (Morak et al, 2013;Stocker et al, 2013;Li et al, 2018).…”

“…Insects thermoregulate behaviorally to control their body temperature, and to avoid overheating and death (Coggan et al, 2011;Kleckova and Klecka, 2016;Abram et al, 2017;Nurme et al, 2018). Adequate information on ambient temperature is of vital importance to exhibit a proper behavioral response but very little is known of the neural pathways and coding of noxious heat by peripheral thermoreceptor neurons in these arthropods (Dhaka et al, 2006;Tang et al, 2013;Must et al, 2017;Nurme et al, 2018). The sensory cells responsible for detection of external temperature are located in various morphological types of cuticular structures on the insect antennae classified as sensilla coeloconica, basiconica, trichodea, styloconica, capitula, coelocapitula, dome shape sensilla, et cetera (Altner and Prillinger, 1980;Altner and Loftus, 1985;Ruchty et al, 2009;Di Giulio et al, 2012;Nagel and Kleineidam, 2015;Zauli et al, 2016;Must et al, 2017;Nurme et al, 2018;Schneider et al, 2018).…”

“…In a sensillum, a single thermoreceptor (cold) neuron usually combines with two antagonistically responding hygroreceptor neurons, the moist air and the dry air neuron, respectively, forming a sensory triad. This classical combination of thermo-and hygroreceptor neurons is widespread in various insect taxa including Blattodea, Coleoptera, Hemiptera, Hymenoptera, Lepidoptera, Odonata, Orthoptera, Phasmatodea (Lacher, 1964;Loftus, 1968;Waldow, 1970;Yokohari and Tateda, 1976;Tichy, 1979;Yokohari et al, 1982;Altner and Loftus, 1985;Nishikawa et al, 1985;Chapman, 1998;Shields and Hildebrand, 1999;Piersanti et al, 2011;Must et al, 2017).…”

“…So far, temperature-sensitive neurons capable of properly encoding noxious heat in the range of 30-45 • C have been demonstrated only in the dome-shaped sensilla (DSS) of two carabid species, Pterostichus oblongopunctatus and Platynus assimilis, respectively (Must et al, 2010(Must et al, , 2017Nurme et al, 2015). The DSSs, earlier also incorrectly termed as campaniform sensilla, occur in small numbers on each antennal flagellomere of many carabid (Merivee et al, 2000(Merivee et al, , 2001(Merivee et al, , 2002Di Giulio et al, 2012) and elaterid beetles (Merivee et al, 1997(Merivee et al, , 1998(Merivee et al, , 1999Zauli et al, 2016).…”

“…By their response modality and reaction type, the three antennal DSS neurons of carabids and elaterids are classified as the unimodal cold-hot neuron (CHN), the bimodal moist-hot neuron (MHN), and the bimodal dry-hot neuron (DHN), respectively (Nurme et al, 2015;Must et al, 2017). In earlier literature, these neurons are termed as the cold neuron, the moist neuron, and the dry neuron, respectively (Merivee et al, 2003(Merivee et al, , 2010Must et al, 2006a,b).…”