Significance We describe a quantitative and robust definition of a brain state as an ensemble of “metastable substates,” each with a probabilistic stability and occurrence frequency. Fitting this to a generative whole-brain model provides an innovative avenue for predicting where simulated brain stimulation can force transitions between different brain states. We provide proof-of-concept by systematically applying this model framework to neuroimaging data of the human sleep cycle and show where to stimulate to awaken the human sleeping brain and vice versa. These results suggest an avenue for using causal whole-brain models to discover in silico where to force a transition between brain states, which may potentially support recovery in disease.