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Slowness of thought is not necessarily a handicap but could be a signature of optimal brain function. Emerging evidence shows that neuroanatomical and dynamical constraints of the human brain shape its functionality in optimal ways, characterized by slowness during task-based cognition in the context of spontaneous resting-state activity. This activity can be described mechanistically by whole-brain computational modeling that relates directly to optimality in the context of theories arguing for metastability in the brain. We discuss the role for optimal processing of information in the context of cognitive, task-related activity, and propose that combining multi-modal neuroimaging and explicit whole-brain models focused on the timing of functional dynamics can help to uncover fundamental rules of brain function in health and disease.