A vast number of different neuronal activity patterns could each induce a different set of activity-regulated genes. Mapping this coupling between activity pattern and gene induction would allow inference of a neuron’s activity-pattern history from its gene expression and improve our understanding of activity-pattern-dependent synaptic plasticity. In genome-scale experiments comparing brief and sustained activity patterns, we reveal that activity-duration history can be inferred from gene expression profiles. Brief activity selectively induces a small subset of the activity-regulated gene program that corresponds to the first of three temporal waves of genes induced by sustained activity. Induction of these first-wave genes is mechanistically distinct from that of the later waves because it requires MAPK/ERK signaling but does not require de novo translation. Thus, the same mechanisms that establish the multi-wave temporal structure of gene induction also enable different gene sets to be induced by different activity durations. Display omitted •Distinct durations of neuronal activity induce different gene expression profiles•Neuronal activity history can be inferred from gene expression•Brief activity induces a gene set defined by sensitivity to MAPK/ERK signaling•H3K27ac and eRNA induction are two separable steps of enhancer activation Tyssowski et al. report that different durations of neuronal activity induce different gene expression profiles, enabling inference of past neuronal activity from gene expression data. Furthermore, they show that MAPK/ERK signaling partially establishes this activity-pattern-to-gene-induction coupling.