Neuroscience Graduate Program, University of California, San Francisco, San Francisco, United States; Neurology Service, San Francisco Veterans Affairs Medical Center, San Francisco, United States; Department of Neurology, University of California, San Francisco, San Francisco, United States; Istituto Italiano di Tecnologia, Rovereto, Italy
Dhakshin S Ramanathan
Department of Psychiatry, University of California, San Diego, San Diego, United States
David Darevksy
Neurology Service, San Francisco Veterans Affairs Medical Center, San Francisco, United States; Department of Neurology, University of California, San Francisco, San Francisco, United States
Daniel Egert
Department of Neurology, University of California, San Francisco, San Francisco, United States
Department of Neurology, University of California, San Francisco, San Francisco, United States; Weill Institute for Neurosciences and Kavli Institute for Fundamental Neuroscience, University of California, San Francisco, San Francisco, United States
Neurology Service, San Francisco Veterans Affairs Medical Center, San Francisco, United States; Department of Neurology, University of California, San Francisco, San Francisco, United States; Weill Institute for Neurosciences and Kavli Institute for Fundamental Neuroscience, University of California, San Francisco, San Francisco, United States
The strength of cortical connectivity to the striatum influences the balance between behavioral variability and stability. Learning to consistently produce a skilled action requires plasticity in corticostriatal connectivity associated with repeated training of the action. However, it remains unknown whether such corticostriatal plasticity occurs during training itself or ‘offline’ during time away from training, such as sleep. Here, we monitor the corticostriatal network throughout long-term skill learning in rats and find that non-rapid-eye-movement (NREM) sleep is a relevant period for corticostriatal plasticity. We first show that the offline activation of striatal NMDA receptors is required for skill learning. We then show that corticostriatal functional connectivity increases offline, coupled to emerging consistent skilled movements, and coupled cross-area neural dynamics. We then identify NREM sleep spindles as uniquely poised to mediate corticostriatal plasticity, through interactions with slow oscillations. Our results provide evidence that sleep shapes cross-area coupling required for skill learning.
