During sleep, the thalamus generates a characteristic pattern of transient, 11-15 Hz sleep spindle oscillations, which synchronize the cortex through large-scale thalamocortical loops. Spindles have been increasingly demonstrated to be critical for sleep-dependent consolidation of memory, but the specific neural mechanism for this process remains unclear. We show here that cortical spindles are spatiotemporally organized into circular wave-like patterns, organizing neuronal activity over tens of milliseconds, within the timescale for storing memories in large-scale networks across the cortex via spike-time dependent plasticity. These circular patterns repeat over hours of sleep with millisecond temporal precision, allowing reinforcement of the activity patterns through hundreds of reverberations. These results provide a novel mechanistic account for how global sleep oscillations and synaptic plasticity could strengthen networks distributed across the cortex to store coherent and integrated memories. DOI: http://dx.doi.org/10.7554/eLife.17267.001