Self-generation of goal-directed choices in a distributed dopaminergic andprefrontal circuit

Abstract

Goal-directed choices that are not triggered by external cues arise from internal representations of the outcomes. The use of a stimulus to specify when to act, which option to take, or whether to explore, has led to consider the reward circuit as a feedforward set of modules carrying independent computations. Here, we develop an uncued task in which mice 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 firing in the ventral tegmental area (VTA), orbitofrontal (OFC) and prefrontal cortices (PFC) that co-encodes and co-determines self-initiation and choices. This sequence appeared with learning as an unguided realignment of spontaneous dynamics. The interactions between the structures depended on the reward context, in particular regarding the uncertainty associated with the different options. We suggest that self-generated choices arise from a distributed circuit based on an OFC-VTA core setting whether to wait or to initiate actions, while the PFC is specifically engaged by reward uncertainty to participate in both the selection and pace of actions. HighlightsO_LISelf-paced actions arise from contextual reorganization of mesocortical dynamics. C_LIO_LIVTA, PFC and OFC complementarily encode predictions and errors about outcomes. C_LIO_LIDistributed firing-then-oscillations dynamics set the goal, initiation and pace of actions. C_LIO_LIVTA and PFC antagonistically promote and inhibit motivation by reward uncertainty. C_LI