Cortical reliability amid noise and chaos

Typical responses of cortical neurons to identical sensory stimuli are highly variable. It has thus been proposed that the cortex primarily uses a rate code. However, other studies have argued for spike-time coding under certain conditions. The potential role of spike-time coding is constrained by the intrinsic variability of cortical circuits, which remains largely unexplored. Here, we quantified this intrinsic variability using a biophysical model of rat neocortical microcircuitry with biologically realistic noise sources. We found that stochastic neurotransmitter release is a critical component of this variability, which, amplified by recurrent connectivity, causes rapid chaotic divergence with a time constant on the order of 10-20 milliseconds. Surprisingly, weak thalamocortical stimuli can transiently overcome the chaos, and induce reliable spike times with millisecond precision. We show that this effect relies on recurrent cortical connectivity, and is not a simple effect of feed-forward thalamocortical input. We conclude that recurrent cortical architecture supports millisecond spike-time reliability amid noise and chaotic network dynamics, resolving a long-standing debate.