Neural reactivations during sleep determine network credit assignment

A fundamental goal of motor learning is to establish neural patterns that produce a desired behavioral outcome. It remains unclear how and when the nervous system solves this “credit–assignment” problem. Using neuroprosthetic learning where we could control the causal relationship between neurons and behavior, here we show that sleep–dependent processing is required for credit-assignment and the establishment of task-related functional connectivity reflecting the casual neuron-behavior relationship. Importantly, we found a strong link between the microstructure of sleep reactivations and credit assignment, with downscaling of non–causal activity. Strikingly, decoupling of spiking to slow–oscillations using optogenetic methods eliminated rescaling. Thus, our results suggest that coordinated firing during sleep plays an essential role in establishing sparse activation patterns that reflect the causal neuron–behavior relationship.