Neuromodulator-induced temperature robustness in a motor pattern: a comparative study between three decapod crustaceans

Abstract

AbstractTemperature fluctuations pose significant challenges to the nervous system, in particular in poikilothermic animals that lack active temperature regulation. Nevertheless, many vital neuronal systems in these animals function over a broad temperature range, making them ideal to study the mechanisms of temperature robustness. Using the gastric mill pattern generator in the Jonah crab,Cancer borealis, we previously demonstrated that temperature-induced increases in membrane leak conductance disrupt neuronal function, but also that neuropeptide modulation provided thermal protection by countering the temperature-induced leak currents. In this study, we test the hypothesis that temperature compensation via neuropeptide modulation is evolutionarily conserved, and not idiosyncratic to Jonah crabs.Our results show that increasing temperature halted rhythmic gastric mill activity in three different crab species (Cancer borealis,Cancer magister,Carcinus maenas). Intracellular recordings revealed temperature-dependent changes in resting membrane potential, action potential amplitude, and postsynaptic potential amplitude. As predicted, higher temperatures diminished LG input resistance, and increasing descending projection neuron activity or applying neuropeptide modulators re-established and rescued rhythms at elevated temperatures.InC. borealisandC. magister, we tested whether the observed changes in input resistance were sufficient to explain the termination of the rhythm at elevated temperature by altering input resistance with dynamic clamp. InC. borealis, decreasing input resistance at cold temperatures terminated rhythms, while increasing it at higher temperatures restored them, demonstrating the critical role of input resistance in temperature-induced rhythm crashes. InC. magister, this approach was successful in about half of the animals, suggesting that additional temperature-induced properties contributed to the termination of the rhythm at elevated temperature.In summary, neuropeptide modulation rescued the gastric mill rhythm in all species, although the underlying cellular properties that caused the temperature crash may be distinct. Our study highlights the potential universality of neuropeptide-mediated temperature compensation.