Neuronal oscillator robustness to multiple global perturbations

Abstract

Neuronal activity depends on ion channels and biophysical processes that are strongly and differentially sensitive to physical variables such as temperature and pH. Nonetheless, neuronal oscillators can be surprisingly resilient to perturbations in these variables. We study a three-neuron pacemaker ensemble that drives the pyloric rhythm of the crab, Cancer borealis. These crabs routinely experience a number of global perturbations, including changes in temperature and pH. Although pyloric oscillations are robust to such changes, for sufficiently large deviations the rhythm reversibly breaks down. As temperature increases beyond a tipping point, oscillators transition to silence. Acidic pH deviations also show tipping points, with a reliable transition first to tonic spiking, then to silence. Surprisingly, robustness to perturbations in pH only moderately affects temperature robustness. Consistent with high animal-to-animal variability in biophysical circuit parameters, tipping points in temperature and pH vary across animals. However, the ordering and discrete classes of transitions at critical points are conserved. This implies that qualitative oscillator dynamics are preserved across animals despite high quantitative parameter variability. A universal model of bursting dynamics predicts the existence of these transition types and the order in which they occur.