Gene expression is heavily controlled at the level of mRNA translation into protein, allowing for stimulus-dependent and compartment-specific activation of protein synthesis. In neurons, mRNA transport to dendrites and axons and local translation are crucial for development, repair, synaptic function and memory formation.3’ untranslated regions (3’UTRs) are known for regulation of RNA localization, stability and translation. Past research identified many of the molecular mechanisms and players involved, but we still lack a systematic understanding of how the regulatory information is encoded in the 3’UTR. Here, we developed a novel massively parallel reporter assay that allows precise measurement of the effect of a 3’UTR sequence on translational output. We tested 13,000 3’UTR sequences from >300 neuronal genes for their ability to regulate RNA translation in neuronal cells and identified many previously unknown regions involved in translational control. To explore the coordination between different gene regulatory layers, we compared the effect of 3’UTRs on translation to their ability to alter RNA stability and localization. We identified 3’UTR regions regulating specifically one regulatory mechanism. However, many RNA localization elements also functioned as translational repressors, hinting at a common regulatory machinery mediating RNA transport and translational repression. Applying our novel MPRA on soma and neurite compartments now allows us to measure local protein synthesis and decipher the rules of compartment-dependent translational control. Knowledge about the sequence basis of neuronal gene regulation can shed light on how mutations interfere with the complex regulatory mechanisms and lead to pathologies.