Synchrony Makes Neurons Fire in Sequence, and Stimulus Properties Determine Who Is Ahead

The synchronized activity of cortical neurons often features spike delays of several milliseconds. Usually, these delays are considered too small to play a role in cortical computations. Here, we use simultaneous recordings of spiking activity from up to 12 neurons to show that, in the cat visual cortex, the pairwise delays between neurons form a preferred order of spiking, called firing sequence. This sequence spans up to similar to 15 ms and is referenced not to external events but to the internal cortical activity (e. g., beta/gamma oscillations). Most importantly, the preferred sequence of firing changed consistently as a function of stimulus properties. During beta/gamma oscillations, the reliability of firing sequences increased and approached that of firing rates. This suggests that, in the visual system, short-lived spatio-temporal patterns of spiking defined by consistent delays in synchronized activity occur with sufficient reliability to complement firing rates as a neuronal code.