Circular RNAs (circRNAs) exhibit unique properties due to their covalently closed nature. Models of circRNAs synthesis and function are emerging, with some known to be translated or act as microRNA sponges, but much about the biogenesis and functions of this surprisingly prevalent class of RNA remains undefined. We identify exonic circRNAs from human and mouse RNA-sequencing datasets, documenting multiple new examples. Applying stringent criteria, we find miRNA binding sites only in a minority of circRNAs and potent ‘sponging’ of a single microRNA by a single circRNA is scarce. Nevertheless, we detect potential for groups of circRNAs acting as ‘distributed’ microRNA sponges. Multiple circRNAs co-sediment with ribosomes, indicative of translation potential. Consistently, we find these circRNAs to be enriched for short open reading frames started by CUG and GUG codons. CircRNAs typically span few exons and their host genes show a pronounced preference for early back-spliced acceptor position and long flanking introns. Analysis of RNA polymerase II (Pol II) occupancy reveals distinctive transcription dynamics. Overall, Pol II traverses circRNA producing regions at accelerated speeds, but shows pronounced pausing over the back-splicing acceptor site. These features likely represent kinetic preconditions for circRNA production that are augmented by looping interactions between flanking introns.