Circular RNAs are enriched in the mammalian brain and are upregulated in response to neuronal differentiation and depolarisation. These RNA molecules, formed by non-canonical back-splicing, have both regulatory and translational potential. Here we carried out an extensive characterisation of circRNA expression in the human brain, in nearly two-hundred human brain samples, from healthy individuals and autism cases. We identify thousands of novel circRNAs, characterise inter-individual variability of circRNA expression in the human brain, and identify brain-region specific circRNAs. We demonstrate that similarly to mRNAs, circRNA isoforms are not expressed stochastically, but rather as major isoforms, supporting their regulated expression in the human brain. We also find that circRNA expression is dynamic during brain development, decreasing with cellular maturation in brain organoids, but remains stable across the adult lifespan. These data provide a comprehensive catalogue of circRNAs and a deeper insight into their expression in the human brain.