During systems consolidation, memories are spontaneously replayed favoring information transfer from hip-pocampus to neocortex. However, at present no empirically supported mechanism to accomplish a transfer of memory from hippocampal to extra-hippocampal sites has been offered. We used cultured neuronal net-works on multi electrode arrays and small scale computational models to study the effect of memory replay on the formation of memory traces. We show that input deprived networks develop an activityconnectivity balance where dominant activity patterns support current connectivity. Electrical stimulation at one electrode disturbs this balance and induces connectivity changes. Intrinsic forces in recurrent networks lead to a new equilibrium, with activity patterns that include the stimulus response. The new connectivity is no longer dis-rupted by this stimulus, indicating that networks memorize it. A different stimulus again induces connectivity changes upon first application but not subsequently, demonstrating the formation of a second memory trace. Returning to the first stimulus doesn’t affect connectivity, indicating parallel storage of both traces. A comput-er model robustly reproduced experimental results, suggesting that STDP and STD suffice to store parallel memory traces, even in networks without particular circuitry constraints.