Abstract
Many species of cold-blooded animals experience substantial and rapid fluctuations in body temperature. Because biological processes are differentially temperature dependent, it is difficult to understand how physiological processes in such animals can be temperature robust [1–8]. Experiments have shown that core neural circuits, such as the pyloric circuit of the crab stomatogastric ganglion (STG), exhibit robust neural activity in spite of large (20°C) temperature fluctuations [3, 5, 7, 8]. This robustness is surprising because (1) each neuron has many different kinds of ion channels with different temperature dependencies (Q10s) that interact in a highly nonlinear way to produce firing patterns and (2) across animals there is substantial variability in conductance densities that nonetheless produce almost identical firing properties. The high variability in conductance densities in these neurons [9, 10] appears to contradict the possibility that robustness is achieved through precise tuning of key temperature-dependent processes. In this paper, we develop a theoretical explanation for how temperature robustness can emerge from a simple regulatory control mechanism that is compatible with highly variable conductance densities [11–13]. The resulting model suggests a general mechanism for how nervous systems and excitable tissues can exploit degenerate relationships among temperature-sensitive processes to achieve robust function.
•Neural activity is generically highly temperature sensitive•Neurons achieve temperature robustness with highly variable conductance densities•Feedback regulation shapes variability to permit temperature-robust neural activity•Robustness to global perturbations constrains cellular regulation mechanisms
All biochemical processes, including neuronal activity, are temperature sensitive. Yet many animal species experience large temperature fluctuations. O’Leary and Marder show how a simple regulatory control mechanism can ensure temperature-robust neural activity by balancing expression of multiple temperature-dependent ion channel types.