Modulations in motor cortical beta and alpha activity have been implicated in the preparation, execution, and termination of voluntary movements. The functional role of motor cortex beta activity is yet to be defined, though two opposing theories prevail. The idling cortex theory suggests that large-scale motor networks, in the absence of input, revert to an intrinsic oscillatory state. The alternative theory proposes that beta activity promotes postural tone at the expense of voluntary movement. These theories are primarily based on observations of event-related desynchronization associated with movement onset. Here, we explore the changes in alpha and beta oscillatory activity associated with the specific behavioral patterns during an established directional uncertainty paradigm. We demonstrate that, consistent with current proposals, alpha and beta desynchronization reflects a process of disengagement from existing networks to enable the creation of functional assemblies. We demonstrate that, following desynchronization, a novel signature of transient alpha synchrony underlies the recruitment of functional assemblies required for directional control. Although alpha and beta desynchronization are dependent upon the number of cues presented, they are not predictive of movement preparation. However, the transient alpha synchrony occurs only when participants have sufficient information to prepare for movement and shows a direct relationship with behavioral performance measures.