Selective coupling and decoupling prepare distributed brain networks for skilled action

Abstract

The precise and rapid nature of skilled actions has motivated a long-standing theory that preparatory neural states must emerge to enable upcoming actions. This has been best characterized in motor cortex, where neural activity evolves toward an initial state that governs subsequent cortical dynamics. Yet complex actions require coordination across multiple areas beyond motor cortex, and how this distributed network prepares remains unknown. We recorded over 40,000 neurons across the brain as mice produced skilled reach-to-grasp actions, revealing selective coupling of action-informative neurons and decoupling of non-informative neurons over a longer timescale and across a broader network than typically associated with motor preparation. These dynamics predicted upcoming action quality and neural activity on individual trials, and performance was impaired when trials were initiated before coupling and decoupling emerged. Two local field potential rhythms organized these dynamics, providing a target for optogenetic intervention that bidirectionally altered action quality. Our work reveals a distributed preparatory process in which selective coupling and decoupling establish a network state that enables skilled action.