We used functional magnetic resonance imaging to examine neuronal activity reflecting the dynamic interplay of external and internal guidance of action. Participants performed a choice reaction time task based on spatial visual cues with their right and left middle and index finger. In a given trial, the cue either fully determined the motor response (no-selection) or indicated the number and location of alternative responses (selection). Compared with fully determined responses, the selection among (two to four) alternative responses activated a widespread bilateral parieto-premotor-prefrontal cortical network along with the cerebellum. Within this network, task-related activity patterns allowed to delineate two sets of brain areas. In the anterior part of rostral dorsal premotor cortex (PMd), the rostral cingulate and supplementary motor area and the right dorsolateral prefrontal cortex, the increase in activity was independent of spatially defined restrictions. In contrast, there was an additional increase in activity in the posterior part of rostral PMd, superior parietal lobule and parieto-occipital sulcus bilaterally as well as in the right anterior intraparietal sulcus, when the visuospatial cue imposed specific constraints on response selection. We propose that the latter set of dorsal parieto-frontal areas subserves rapid implementation of spatial information during visually guided response selection.