Motion transparency is the perception of multiple, moving surfaces within the same retinal location (for example, a ripple on the surface of a drifting stream), and is an interesting challenge to motion models because multiple velocities must be represented within the same region of space. When these motion vectors are in opposite directions, brief in duration and spatially constrained within a very local region, the result is little or no perceived motion (motion opponency). Both motion transparency and motion opponency inhibit the firing rate of single middle temporal area (MT) neurons as compared with the preferred direction alone, but neither generally influences the firing rate of primary visual cortex neurons. Surprisingly, neuroimaging studies of human middle temporal area (hMT+) have found less activation due only to motion opponency and an increase in neural responses for motion transparency. Here we parametrically manipulate the local balance between competing motion vectors and find an interaction between motion opponency and transparency in the population blood oxygen level-dependent (BOLD) response. We find reduced BOLD amplitude for motion opponency throughout visual cortex, but weakened responses due to perceptual transparency that is most apparent only within the hMT+. We interpret our results as evidence for two distinct mechanisms mediating opponency and transparency.