In monkeys, neurons in the hand representation of the primary motor cortex (M1) are often tuned to the direction of hand movement, and there is evidence that these neurons are clustered according to their “preferred” direction of movement. However, this organizational principle has yet to be demonstrated in M1 of humans. We conducted a functional magnetic resonance imaging (fMRI) study in which participants used a joystick to move a cursor from a central origin to one of five equidistant targets. The fMRI signal of individual voxels was sensitive to the directional aspects of the reaching task and manifested direction-specific adaptation. Furthermore, the correlation between multivoxel patterns of responses for different movement directions depended on the angular distance between them. We conclude that M1 neurons are likely to be organized in clusters according to their preferred direction, since only such a coarse-grained representation can lead to directional selectivity of voxels, encompassing millions of neurons. A simple model that estimates cluster size suggests that the diameter of these clusters is on the order of a few hundred micrometers.