Any motor action results from a dynamic interplay of various brain regions involved in different aspects of movement preparation and execution. Establishing a reliable model of how these areas interact is crucial for a better understanding of the mechanisms underlying motor function in both healthy subjects and patients. We used fMRI and dynamic causal modeling to reveal the specific excitatory and inhibitory influences within the human motor system for the generation of voluntary hand movements. We found an intrinsic balance of excitatory and inhibitory couplings among core motor regions within and across hemispheres. Neural coupling within this network was specifically modulated upon uni- and bimanual movements. During unimanual movements, connectivity towards the contralateral primary motor cortex was enhanced while neural coupling towards ipsilateral motor areas was reduced by both transcallosal inhibition and top-down modulation. Bimanual hand movements were associated with a symmetric facilitation of neural activity mediated by both increased intrahemispheric connectivity and enhanced transcallosal coupling of SMA and M1. The data suggest that especially the supplementary motor area represents a key structure promoting or suppressing activity in the cortical motor network driving uni- and bilateral hand movements. Our data demonstrate that fMRI in combination with DCM allows insights into intrinsic properties of the human motor system and task-dependent modulations thereof.