We have identified a specific set of experienced-dependent lncRNAs that accumulate in the synaptic compartment within the infralimbic prefrontal cortex of adult male C57/Bl6 mice. Among these was a splice variant related to the stress-associated lncRNA, Gas5. RNA immunoprecipitation followed by mass spectrometry and single-molecule imaging revealed that this Gas5 isoform, in association with the RNA binding proteins G3bp2 and Caprin1, regulates the activity-dependent trafficking and clustering of RNA granules. We also identified an m6A-modified variant of Malat1 in the synaptic compartment that interacts with previously uncharacterised m6A-readers, including cytoplasmic FMR1 interacting protein 2 (CYFIP2) and dihydropyrimidase-related protein 2 (DPYSL2). These findings reveal new mechanisms of memory that involve the dynamic interaction between lncRNA activity, RNA condensates and novel m6A-readers at synapse.