Dopaminergic and prefrontal dynamics co-determine mouse decisions in a spatial gambling task
Elise Bousseyrol,
Steve Didienne,
Samir Takillah,
Clement Prevost-Solié,
Maxime Come,
Tarek Ahmed Yahia,
Sarah Mondoloni,
Eléonore Vicq,
Ludovic Tricoire,
Alexandre Mourot,
Jérémie Naudé,
Philippe Faure
Affiliations
Elise Bousseyrol
Sorbonne Université, INSERM, CNRS, Neuroscience Paris Seine – Institut de Biologie Paris Seine (NPS – IBPS), 75005 Paris, France; Brain Plasticity Laboratory, CNRS, ESPCI Paris, PSL Research University, 75005 Paris, France
Steve Didienne
Sorbonne Université, INSERM, CNRS, Neuroscience Paris Seine – Institut de Biologie Paris Seine (NPS – IBPS), 75005 Paris, France; Brain Plasticity Laboratory, CNRS, ESPCI Paris, PSL Research University, 75005 Paris, France
Samir Takillah
Sorbonne Université, INSERM, CNRS, Neuroscience Paris Seine – Institut de Biologie Paris Seine (NPS – IBPS), 75005 Paris, France; Brain Plasticity Laboratory, CNRS, ESPCI Paris, PSL Research University, 75005 Paris, France
Clement Prevost-Solié
Sorbonne Université, INSERM, CNRS, Neuroscience Paris Seine – Institut de Biologie Paris Seine (NPS – IBPS), 75005 Paris, France; Brain Plasticity Laboratory, CNRS, ESPCI Paris, PSL Research University, 75005 Paris, France
Maxime Come
Sorbonne Université, INSERM, CNRS, Neuroscience Paris Seine – Institut de Biologie Paris Seine (NPS – IBPS), 75005 Paris, France; Brain Plasticity Laboratory, CNRS, ESPCI Paris, PSL Research University, 75005 Paris, France
Tarek Ahmed Yahia
Sorbonne Université, INSERM, CNRS, Neuroscience Paris Seine – Institut de Biologie Paris Seine (NPS – IBPS), 75005 Paris, France
Sarah Mondoloni
Sorbonne Université, INSERM, CNRS, Neuroscience Paris Seine – Institut de Biologie Paris Seine (NPS – IBPS), 75005 Paris, France
Eléonore Vicq
Sorbonne Université, INSERM, CNRS, Neuroscience Paris Seine – Institut de Biologie Paris Seine (NPS – IBPS), 75005 Paris, France
Ludovic Tricoire
Sorbonne Université, INSERM, CNRS, Neuroscience Paris Seine – Institut de Biologie Paris Seine (NPS – IBPS), 75005 Paris, France
Alexandre Mourot
Sorbonne Université, INSERM, CNRS, Neuroscience Paris Seine – Institut de Biologie Paris Seine (NPS – IBPS), 75005 Paris, France; Brain Plasticity Laboratory, CNRS, ESPCI Paris, PSL Research University, 75005 Paris, France
Jérémie Naudé
Sorbonne Université, INSERM, CNRS, Neuroscience Paris Seine – Institut de Biologie Paris Seine (NPS – IBPS), 75005 Paris, France; CNRS, Université de Montpellier, INSERM – Institut de Génomique Fonctionnelle, 34094 Montpellier, France; Corresponding author
Philippe Faure
Sorbonne Université, INSERM, CNRS, Neuroscience Paris Seine – Institut de Biologie Paris Seine (NPS – IBPS), 75005 Paris, France; Brain Plasticity Laboratory, CNRS, ESPCI Paris, PSL Research University, 75005 Paris, France; Corresponding author
Summary: 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.
