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In the striatum, signaling via G protein-coupled neurotransmitter receptors is essential for motor control. Critical to this process is the effector enzyme adenylyl cyclase type 5 (AC5) that produces second messenger cAMP upon receptor-mediated activation by G protein Golf. However, the molecular organization of the Golf-AC5 signaling axis is not well understood. In this study, we report that in the striatum AC5 exists in a stable pre-coupled complex with subunits of Golf heterotrimer. We use genetic mouse models with disruption in individual components of the complex to reveal hierarchical order of interactions required for AC5-Golf stability. We further identify that the assembly of AC5-Golf complex is mediated by PhLP1 chaperone that plays central role in neurotransmitter receptor coupling to cAMP production motor learning. These findings provide evidence for the existence of stable G protein-effector signaling complexes and identify a new component essential for their assembly. DOI: http://dx.doi.org/10.7554/eLife.10451.001, eLife digest In the brain, cells called neurons communicate with one another using chemicals called neurotransmitters, which bind to receptors on the surface of cells. In most cases, the binding of neurotransmitter causes a protein known as a G protein to interact with the receptor. G proteins are made up of three subunits: α, β and γ. After binding to the receptor, the α subunit separates from the β/γ subunits – which remain together – and both components then act as signals to activate specific targets in the cell. There are many different α, β and γ subunits, which participate in various signaling pathways in different parts of the brain. In the striatum – a region involved in controlling movement – a particular combination of α, β and γ subunits called Golf is responsible for activating an enzyme called adenylyl cyclase type 5 (AC5). Traditionally, G protein signalling has been thought to occur in stages so that the binding of neurotransmitter to receptors on striatal neurons would lead to the dissociation of Golf into the α and βγ subunits. Then the α and βγ subunits are thought to bind to and activate AC5. However, Xie et al. now show that all three subunits of Golf are already found in a stable group (or complex) with AC5 in striatal neurons. Neurotransmitter binding to the receptors causes the entire Golf-AC5complex to rearrange and this process activates AC5. A particular chaperone protein regulates the assembly of the G protein-AC5complex. Mice that lack the gene that encodes this chaperone in striatal neurons struggle to learn how to balance on a rotating rod. In humans, mutations in the genes that encode Golf and AC5 cause dystonia, which is a disorder characterised by involuntary movements. Given the evidence linking this chaperone protein to the regulation of Golf-AC5 signaling, future experiments should investigate whether it might also contribute to dystonia. DOI: http://dx.doi.org/10.7554/eLife.10451.002