Cortical motor maps are the basis of voluntary movement, but they have proven difficult to understand in the context of their underlying neuronal circuits. We applied light-based motor mapping of Channelrhodopsin-2 mice to reveal a functional subdivision of the forelimb motor cortex based on the direction of movement evoked by brief (10 ms) pulses. Prolonged trains of electrical or optogenetic stimulation (100–500 ms) targeted to anterior or posterior subregions of motor cortex evoked reproducible complex movements of the forelimb to distinct positions in space. Blocking excitatory cortical synaptic transmission did not abolish basic motor map topography, but the site-specific expression of complex movements was lost. Our data suggest that the topography of movement maps arises from their segregated output projections, whereas complex movements evoked by prolonged stimulation require intracortical synaptic transmission. ► Optogenetic mapping reveals functional subdivision of mouse forelimb motor cortex ► Prolonged stimulation evokes distinct complex movements from different cortical areas ► Complex movements require cortical synaptic transmission, but map topography does not ► Movement representations have separate corticofugal projections Using light to stimulate the mouse brain, Harrison et al. identify brain areas responsible for producing different types of forelimb movements and study the function of circuits within those areas by locally blocking communication between neurons.