Neural Code for Ambient Heat Detection in Elaterid Beetles.

Enno Merivee,Karin Nurme,Marika Mänd,Maurizio Muzzi,Andrea Di Giulio,Anne Must,Ingrid Williams

doi:10.3389/fnbeh.2020.00001

Abstract

Environmental thermal conditions play a major role at all levels of biological organization; however, there is little information on noxious high temperature sensation crucial in behavioral thermoregulation and survival of small ectothermic animals such as insects. So far, a capability to unambiguously encode heat has been demonstrated only for the sensory triad of the spike bursting thermo- and two bimodal hygro-thermoreceptor neurons located in the antennal dome-shaped sensilla (DSS) in a carabid beetle. We used extracellular single sensillum recording in the range of 20–45°C to demonstrate that a similar sensory triad in the elaterid Agriotes obscurus also produces high temperature-induced bursty spike trains. Several parameters of the bursts are temperature dependent, allowing the neurons in a certain order to encode different, but partly overlapping ranges of heat up to lethal levels in a graded manner. ISI in a burst is the most useful parameter out of six. Our findings consider spike bursting as a general, fundamental quality of the classical sensory triad of antennal thermo- and hygro-thermoreceptor neurons widespread in many insect groups, being a flexible and reliable mode of coding unfavorably high temperatures. The possible involvement of spike bursting in behavioral thermoregulation of the beetles is discussed. By contrast, the mean firing rate of the neurons in regular and bursty spike trains combined does not carry useful thermal information at the high end of noxious heat.

Highlights

Environmental thermal conditions play a major role at all levels of biological organization
We show, for the first time, that high temperature-induced, temperature-dependent spike burst patterns of the sensory triad occur in insect taxa other than Carabidae
Our electrophysiological experiments with the classical sensory triad of thermo- and hygroreceptor neurons in the antennal dome-shaped sensilla (DSS) of the elaterid beetle, A. obscurus, showed that even though mean firing rate of the unimodal cold-hot neuron (CHN) unambiguously depends on temperature in the range of 20–35◦C, above that range, the parameter stabilizes at about 10 spikes s−1

Summary

Introduction

Environmental thermal conditions play a major role at all levels of biological organization. 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). Data about heat reception in insects is still insufficient (Dhaka et al, 2006; Abram et al, 2017)

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Conclusion