Synapses are specialized contact loci between neurons and partner cells, which ensure directed communication between the two. A characteristic feature of chemical synapses is the change in strength of the synaptic connection upon activity. This process, called synaptic plasticity, enables synapses to regulate the information flow. Thus, information can be filtered, modified and integrated in different ways at the same synapse, depending on its activation history. This flexibility is thought to be important for higher cognitive functions like learning and memory. Many molecules have been discovered to be essential for synaptic plasticity, while the corresponding molecular mechanisms behind plastic changes remain largely hidden. In the present work, we addressed the question how different activation patterns can alter the same synaptic connection. To evoke longer-lasting synaptic changes in vivo Channelrhodopsin-2 was expressed at the Drosophila neuromuscular junction, namely in three different combinations: presynaptically in the motoneuron, postsynaptically in the muscle, or in both compartments. Using blue light the synapse could now be activated in alive, freely moving Drosophila larvae. Together with electrophysiological recordings, our results show that paired pre- and postsynaptic depolarisations trigger supralinear changes in synaptic function. These appear to be mediated by the specific incorporation of the glutamate receptor subunit GluRIIA.