Summary
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 reports show spike-time coding under certain conditions. The potential role of spike-time coding is constrained by the variability arising directly from noise sources within local cortical circuits. Here, we quantified this internally generated variability using a detailed model of rat neocortical microcircuitry with biologically realistic noise sources. We found stochastic neurotransmitter release to be 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, however, relatively 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 result of feed-forward thalamocortical input. We conclude that recurrent cortical architecture simultaneously supports both chaotic network dynamics and millisecond spike-time reliability.