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The neural mechanisms by which animals initiate goal-directed actions, choose between options, or explore opportunities remain unknown. Here, we develop a spatial gambling task in which mice, to obtain intracranial self-stimulation rewards, self-determine the initiation, direction, vigor, and pace of their actions based on their knowledge of the outcomes. Using electrophysiological recordings, pharmacology, and optogenetics, we identify a sequence of oscillations and firings in the ventral tegmental area (VTA), orbitofrontal cortex (OFC), and prefrontal cortex (PFC) that co-encodes and co-determines self-initiation and choices. This sequence appeared with learning as an uncued realignment of spontaneous dynamics. Interactions between the structures varied with the reward context, particularly the uncertainty associated with the different options. We suggest that self-generated choices arise from a distributed circuit based on an OFC-VTA core determining whether to wait for or initiate actions, while the PFC is specifically engaged by reward uncertainty in action selection and pace. [Display omitted] • Self-paced actions arise from contextual reorganization of mesocortical dynamics • VTA, PFC, and OFC complementarily encode predictions and errors about outcomes • Distributed "firing then oscillations" dynamics set the goal, initiation, and pace of actions • VTA and PFC antagonistically promote and inhibit motivation by reward uncertainty The neural mechanisms by which animals initiate goal-directed behaviors, choose between alternatives, and explore potentially informative ones are far from understood. Using a mouse gambling task, Bousseyrol et al. identified a sequence of oscillations and firings in ventral tegmental, orbitofrontal, and prefrontal areas that jointly encode choice and action. [ABSTRACT FROM AUTHOR]