The brain is a complex, interconnected information processing network. In humans, this network supports a mental workspace that enables high-level abilities such as scientific and artistic creativity. Do the component processes underlying these abilities occur in discrete anatomical modules, or are they distributed widely throughout the brain? How does the flow of information within this network support specific cognitive functions? Current approaches have limited ability to answer such questions. Here, we report novel multivariate methods to analyze information flow within the mental workspace during visual imagery manipulation. We find that mental imagery entails distributed information flow and shared representations throughout the cortex. These findings challenge existing, anatomically modular models of the neural basis of higher-order mental functions, suggesting that such processes may occur at least in part at a fundamentally distributed level of organization. The novel methods we report may be useful in studying other similarly complex, high-level informational processes.