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

Cell. 2019 Apr 18;177(3):669-682.e24. doi: 10.1016/j.cell.2019.02.019. Epub 2019 Mar 28.

Abstract

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.

Keywords: brain state; cerebellum; dimensional expansion; granule cells; layer 5; motor learning; movement planning; neocortex; pontine nuclei; reward.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Behavior, Animal
  • Calcium / metabolism
  • Cerebellum / metabolism*
  • Forelimb / physiology
  • Mice
  • Mice, Transgenic
  • Microscopy, Fluorescence, Multiphoton
  • Neocortex / metabolism*
  • Neocortex / pathology
  • Opsins / genetics
  • Opsins / metabolism
  • Pyramidal Cells / metabolism

Substances

  • Opsins
  • Calcium