Shared Cortex-Cerebellum Dynamics in the Execution and Learning of a Motor Task

Throughout mammalian neocortex, layer 5 pyramidal (L5) cells project via the pons to a vast number of cerebellar granule cells (GrCs), forming a fundamental pathway. Yet, it is unknown how neuronal dynamics are transformed through the L5→GrC pathway. Here, by directly comparing premotor L5 and GrC activity during a forelimb movement task using dual-site two-photon Ca2+ imaging, we found that in expert mice, L5 and GrC dynamics were highly similar. L5 cells and GrCs shared a common set of task-encoding activity patterns, possessed similar diversity of responses, and exhibited high correlations comparable to local correlations among L5 cells. Chronic imaging revealed that these dynamics co-emerged in cortex and cerebellum over learning: as behavioral performance improved, initially dissimilar L5 cells and GrCs converged onto a shared, low-dimensional, task-encoding set of neural activity patterns. Thus, a key function of cortico-cerebellar communication is the propagation of shared dynamics that emerge during learning. [Display omitted] •First simultaneous recordings from neocortex and cerebellum over weeks of learning•Cortical layer 5 and cerebellar granule cells show similar task encoding in experts•Learning increases correlations among initially dissimilar L5 and granule cells•L5 and granule cells converge to similar, low-dimensional, task-encoding activity Simultaneous recordings of ensembles of individual neurons in the neocortex and cerebellum provide a view of how these two brain regions learn together.