Many parameter sets in a multicompartment model oscillator are robust to temperature perturbations

Abstract

Neurons in cold-blooded animals remarkably maintain their function over a wide range of temperatures, even though the rates of many cellular processes increase twofold, threefold, or many-fold for each 10°C increase in temperature. Moreover, the kinetics of ion channels, maximal conductances, and Ca2+ buffering each have independent temperature sensitivities, suggesting that the balance of biological parameters can be disturbed by even modest temperature changes. In stomatogastric ganglia of the crab Cancer borealis, the duty cycle of the bursting pacemaker kernel is highly robust between 7 and 23°C (Rinberg et al., 2013). We examined how this might be achieved in a detailed conductance-based model in which exponential temperature sensitivities were given by Q10 parameters. We assessed the temperature robustness of this model across 125,000 random sets of Q10 parameters. To examine how robustness might be achieved across a variable population of animals, we repeated this analysis across six sets of maximal conductance parameters that produced similar activity at 11°C. Many permissible combinations of maximal conductance and Q10 parameters were found over broad regions of parameter space and relatively few correlations among Q10s were observed across successful parameter sets. A significant portion of Q10 sets worked for at least 3 of the 6 maximal conductance sets (~11.1%). Nonetheless, no Q10 set produced robust function across all six maximal conductance sets, suggesting that maximal conductance parameters critically contribute to temperature robustness. Overall, these results provide insight into principles of temperature robustness in neuronal oscillators. © 2014 the authors.