Critical Slowing Down Governs the Transition to Neuron Spiking

Abstract

Many complex systems have been found to exhibit critical transitions, or so-called tipping points, which are sudden changes to a qualitatively different system state. These changes can profoundly impact the functioning of a system ranging from controlled state switching to a catastrophic break-down; signals that predict critical transitions are therefore highly desirable. To this end, research efforts have focused on utilizing qualitative changes in markers related to a system’s tendency to recover more slowly from a perturbation the closer it gets to the transition—a phenomenon called critical slowing down. The recently studied scaling of critical slowing down offers a refined path to understand critical transitions: to identify the transition mechanism and improve transition prediction using scaling laws.

Here, we outline and apply this strategy for the first time in a real-world system by studying the transition to spiking in neurons of the mammalian cortex. The dynamical system approach has identified two robust mechanisms for the transition from subthreshold activity to spiking, saddle-node and Hopf bifurcation. Although theory provides precise predictions on signatures of critical slowing down near the bifurcation to spiking, quantitative experimental evidence has been lacking. Using whole-cell patch-clamp recordings from pyramidal neurons and fast-spiking interneurons, we show that 1) the transition to spiking dynamically corresponds to a critical transition exhibiting slowing down, 2) the scaling laws suggest a saddle-node bifurcation governing slowing down, and 3) these precise scaling laws can be used to predict the bifurcation point from a limited window of observation. To our knowledge this is the first report of scaling laws of critical slowing down in an experiment. They present a missing link for a broad class of neuroscience modeling and suggest improved estimation of tipping points by incorporating scaling laws of critical slowing down as a strategy applicable to other complex systems.

Author Summary

Neurons efficiently convey information by being able to switch rapidly between two different states: quiescence and spiking. Such sudden shifts to a qualitatively different state are observed in many complex systems; the often dramatic consequences of these tipping points for diverse fields such as economics, ecology, and the brain have spurred interest to better understand their transition mechanisms and predict their sudden occurrences. By studying the transition from neuronal quiescence to spiking, we show that the quantitative scaling laws for critical slowing down, i.e., a system’s tendency to recover more slowly from perturbations upon approaching its transition point, inform about the underlying bifurcation mechanism and can be used to improve the prediction of a system’s tipping point.