Rate coding and spike-time variability in cortical neurons with two types of threshold dynamics

Neurons and dynamical models of spike generation display two different classes of threshold behavior: type 1 [firing frequency vs. current (f-I) relationship is continuous at threshold] and type 2 (discontinuous f-I). With steady current or conductance stimulation, regular-spiking (RS) pyramidal neurons and fast-spiking (FS) inhibitory interneurons in layer 2/3 of somatosensory cortex exhibit type 1 and type 2 threshold behaviors, respectively. We compared the postsynaptic firing variability of type 1 RS and type 2 FS cells, during naturalistic, fluctuating conductance input. In RS neurons, increasing the level of independently random, shunting inhibition caused a monotonic increase in spike reliability, whereas in FS interneurons, there was an optimum level of shunting inhibition for achieving the most reliable spike generation and the most precise spike-time encoding. This was observed over a range of different degrees of synchrony, or correlation, in the input. RS cells displayed a progressive rise in spike jitter during natural-like transient burst inputs, whereas for FS cells, jitter was mostly kept low. Furthermore, RS cells showed encoding of the input level in the spike shape, whereas FS cells did not. These differences between the two cell types are consistent with a role of RS neurons as rate-coding integrators, and a role of FS neurons as resonators controlling the coherence of synchronous firing.