The gene of encodes a highly abundant 47 kDa synaptic vesicle-associated protein. null mutants show defects in synaptic plasticity and larval olfactory associative learning but the molecular function of Sap47 at the synapse is unknown. We demonstrate that Sap47 modulates the phosphorylation of another highly abundant conserved presynaptic protein, synapsin. Site-specific phosphorylation of synapsin has repeatedly been shown to be important for behavioural plasticity but information of where in the brain phospho-synapsin isoforms are localized has been lacking. Here we report the distribution of serine-6-phosphorylated synapsin in the adult brain and show that it is highly enriched in rings of synapses in the ellipsoid body, and in large synapses near the lateral triangle. Effects of knock-out of or on olfactory associative learning/memory are compatible with the hypothesis that both proteins operate in the same molecular pathway. We therefore asked if this might also hold for other aspects of their function. We show that knock-out of but not reduces life span, whereas knock-out of , or both affects climbing as well as plasticity in circadian rhythms and sleep. Furthermore, electrophysiological assessment of synaptic properties at the larval neuromuscular junction (NMJ) reveals increased spontaneous synaptic vesicle fusion and reduced paired pulse facilitation in and single and double mutants. Our results imply that Sap47 and synapsin cooperate non-uniformly in the control of synaptic properties in different behaviourally relevant neuronal networks of the fruitfly.