Although the superior dexterity of one hand is an almost ubiquitous human experience, it is unclear which characteristics of the motor system controlling the preferred hand produce this superior dexterity. Between-species studies show that greater dexterity is associated with a motor system that permits more independent movements of the digits. If between-hand dexterity differences are mediated by the same mechanism as between-species dexterity differences, then there should be asymmetries within the corticospinal tracts of humans that would result in between-hand independence differences. The evidence for asymmetries in the corticospinal tracts is sparse, and if an asymmetry does exist, it appears to be limited to the control of intrinsic hand muscles. We wondered, therefore, whether there might be a difference in the degree of independent control on the two hands during performance of a task that primarily uses intrinsic hand muscles. We examined digit individuation when subjects produced abduction or adduction forces with a single digit in isolation. Consistent with previous studies in which forces or movements in single digits were generated primarily by extrinsic hand muscles, we found no difference between the individuation of the digits on the preferred and non-preferred hands. We suggest that whereas independence differences underlie large dexterity differences between species, they do not underlie the more subtle dexterity differences between the preferred and non-preferred hands. Instead, the neural substrate for handedness might be asymmetrical connectivity within M1, with more profuse connections within the dominant than non-dominant M1 imparting a greater potential for excitatory and inhibitory interactions between movement representations which might then result in the more efficient coordination of hand and arm movements of the preferred hand.