Bursty spike trains of antennal thermo- and bimodal hygrothermoreceptor neurons encode noxious heat in elaterid beetles

The main purpose of this study was to explain the internal fine structure of potential antennal thermo- and hygroreceptive sensilla, their innervation specifics, and responses of the sensory neurons to thermal and humidity stimuli in an elaterid beetle using focused ion beam scanning electron microscopy and electrophysiology, respectively. Several essential, high temperature induced turning points in the locomotion were determined using automated video tracking. Our results showed that the sensilla under study, morphologically, are identical to the domeshaped sensilla (DSS) of carabids. A cold-hot neuron and two bimodal hygro-thermoreceptor neurons, the moist-hot and dry-hot neuron, innervate them. Above 25–30 °C, all the three neurons, at different threshold temperatures, switch from regular spiking to temperature dependent spike bursting. The percentage of bursty DSS neurons on the antenna increases with temperature increase suggesting that this parameter of the neurons may encode noxious heat in a graded manner. Thus, we show that besides carabid beetles, elaterids are another large group of insects with this ability. The threshold temperature of the beetles for onset of elevated locomotor activity (OELA) was lower by 11.9 °C compared to that of critical thermal maximum (39.4 °C). Total paralysis occurred at 41.8 °C. The threshold temperatures for spike bursting of the sensory neurons in DSS and OELA of the beetles coincide suggesting that probably the spike bursts are responsible for encoding noxious heat when confronted. In behavioural thermoregulation, spike bursting DSS neurons serve as a fast and firm three-fold early warning system for the beetles to avoid overheating and death

Responses of the antennal bimodal hygroreceptor neurons to innocuous and noxious high temperatures in the carabid beetle, Pterostichus oblongopunctatus

Electrophysiological responses of thermo- and hygroreceptor neurons from antennal dome-shaped sen- 32 silla of the carabid beetle Pterostichus oblongopunctatus to different levels of steady temperature ranging 33 from 20 to 35 C and rapid step-changes in it were measured and analysed at both constant relative and 34 absolute ambient air humidity conditions. It appeared that both hygroreceptor neurons respond to tem- 35 perature which means that they are bimodal. For the first time in arthropods, the ability of antennal dry 36 and moist neurons to produce high temperature induced spike bursts is documented. Burstiness of the 37 spike trains is temperature dependent and increases with temperature increase. Threshold temperatures 38 at which the two neurons switch from regular spiking to spike bursting are lower compared to that of the 39 cold neuron, differ and approximately coincide with the upper limit of preferred temperatures of the spe- 40 cies. We emphasise that, in contrast to various sensory systems studied, the hygroreceptor neurons of P. 41 oblongopunctatus have stable and continuous burst trains, no temporal information is encoded in the tim- 42 ing of the bursts. We hypothesise that temperature dependent spike bursts produced by the antennal 43 thermo- and hygroreceptor neurons may be responsible for detection of noxious high temperatures 44 important in behavioural thermoregulation of carabid beetles

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

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