During sleep, cortical network connectivity likely undergoes both synaptic potentiation and depression through system consolidation and homeostatic processes. However, how these modifications are coordinated across sleep stages remains largely unknown. Candidate mechanisms are Ponto-Geniculo-Occipital (PGO) waves, propagating across several structures during Rapid Eye Movement (REM) sleep and the transitional stage from non-REM sleep to REM sleep (pre-REM), and exhibiting sleep stage-specific dynamic patterns. To understand their impact on cortical plasticity, we built an acetylcholine-modulated neural mass model of PGO wave propagation through pons, thalamus and cortex, reproducing a broad range of electrophysiological characteristics across sleep stages. Using a population model of Spike-Time-Dependent Plasticity, we show that recurrent cortical circuits in different transient regimes depending on the sleep stage with different impacts on plasticity. Specifically, this leads to the potentiation of cortico-cortical synapses during pre-REM, and to their depression during REM sleep. Overall, our results provide a new view on how transient sleep events and their associated sleep stage may implement a precise control of system-wide plastic changes.