Neural reactivations during sleep determine network credit assignment

• Published in: Nature neuroscience Vol. 20; no. 9; pp. 1277 - 1284
• Main Authors: Gulati, Tanuj, Guo, Ling, Ramanathan, Dhakshin S, Bodepudi, Anitha, Ganguly, Karunesh
• Format: Journal Article
• Language: English
• Published: New York Nature Publishing Group US 01.09.2017; Nature Publishing Group
• Subjects: 631/378/1385; 631/378/2632/2634; 9/30; Action Potentials - physiology; Animal Genetics and Genomics; Animals; Arbitration; Behavioral Sciences; Biological Techniques; Biomedicine; Brain research; Bus drivers; Decoupling; Firing pattern; Male; Motor Cortex - physiology; Motor learning; Motor skill learning; Nerve Net - physiology; Nervous system; Neural circuitry; Neural networks; Neurobiology; Neurons - physiology; Neurosciences; Optogenetics - methods; Oscillations; Prosthetics; Psychological aspects; Rats; Rats, Long-Evans; Rescaling; Scaling; Sleep; Sleep - physiology
• ISSN: 1097-6256; 1546-1726; 1546-1726
• DOI: 10.1038/nn.4601

A fundamental goal of learning is to establish neural patterns that cause desired behaviors. This paper demonstrates that sleep-dependent processing is required for credit assignment and the establishment of task-related activity reflecting the causal neuron-behavior relationship. Decoupling of spiking to sleep slow oscillations using optogenetics methods disrupted this process. A fundamental goal of motor learning is to establish the 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, in which we could control the causal relationship between neurons and behavior, we found that sleep-dependent processing was required for credit assignment and the establishment of task-related functional connectivity reflecting the casual neuron–behavior relationship. Notably, we observed a strong link between the microstructure of sleep reactivations and credit assignment, with downscaling of non-causal activity. Decoupling of spiking to slow oscillations using optogenetic methods eliminated rescaling. Thus, our results suggest that coordinated firing during sleep is essential for establishing sparse activation patterns that reflect the causal neuron-behavior relationship.