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A consistent finding in motor EEG research is a bilateral attenuation of oscillatory activity over sensorimotor regions close to the onset of an upcoming unilateral hand movement. In contrast, little is known about how movement initiation affects oscillatory activity, especially in the hemisphere ipsilateral to the moving hand. We here investigated the neural mechanisms modulating oscillatory activity in the ipsilateral motor cortex prior to movement onset under the control of two different initiating networks, namely, Self-initiated and Visually-cued actions. During motor preparation, a contralateral preponderance of power over sensorimotor cortex (SM) was observed in α and β bands during Visually-cued movements, whereas power changes were more bilateral during Self-initiated movements. Coherence between ipsilateral SM (iSM) and contralateral SM (cSM) in the α-band was significantly increased compared to the respective baseline values, independent of the context of movement initiation. However, this context-independent cSM-iSM coherence modulated the power changes in iSM in a context-dependent manner, that is, a stronger cSM-iSM coherence correlated with a larger decrease in high-β power over iSM in the Self-initiated condition, in contrast to a smaller decrease in α power in the Visually-cued condition. In addition, the context-dependent coherence between SMA and iSM in the α-band and δ-Θ-band for the Self-initiated and Visually-cued condition, respectively, exhibited a similar context-dependent modulation for power changes. Our findings suggest that the initiation of regional oscillations over iSM reflects changes in the information flow with the contralateral sensorimotor and premotor areas dependent upon the context of movement initiation. Importantly, the interaction between regional oscillations and network-like oscillatory couplings indicates different frequency-specific inhibitory mechanisms that modulate the activity in the ipsilateral sensorimotor cortex dependent upon how the movement is initiated.