Different patterns of neuronal activity differentially induce sets of activity-regulated genes (ARGs), but the mechanisms are poorly understood. Here, RNA-sequencing approaches were used to identify ARGs and transcriptional regulators that were induced by different activity patterns in mouse cultured cortical neurons. Different durations of neuronal activation activated specific inducible signalling pathways (including MAPK/ERK) that regulated distinct waves of ARG expression that are each independently coupled to different activity patterns.